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Fomite Transmission Follows Invasion Ecology Principles

The invasion ecology principles illustrated in many ecosystems have not yet been explored in the context of fomite transmission. We hypothesized that invaders in fomite transmission are trackable, are neutrally distributed between hands and environmental surfaces, and exhibit a proximity effect. To...

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Autores principales: Wang, Peihua, Tong, Xinzhao, Zhang, Nan, Miao, Te, Chan, Jack P. T., Huang, Hong, Lee, Patrick K. H., Li, Yuguo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9238404/
https://www.ncbi.nlm.nih.gov/pubmed/35502902
http://dx.doi.org/10.1128/msystems.00211-22
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author Wang, Peihua
Tong, Xinzhao
Zhang, Nan
Miao, Te
Chan, Jack P. T.
Huang, Hong
Lee, Patrick K. H.
Li, Yuguo
author_facet Wang, Peihua
Tong, Xinzhao
Zhang, Nan
Miao, Te
Chan, Jack P. T.
Huang, Hong
Lee, Patrick K. H.
Li, Yuguo
author_sort Wang, Peihua
collection PubMed
description The invasion ecology principles illustrated in many ecosystems have not yet been explored in the context of fomite transmission. We hypothesized that invaders in fomite transmission are trackable, are neutrally distributed between hands and environmental surfaces, and exhibit a proximity effect. To test this hypothesis, a surrogate invader, Lactobacillus delbrueckii subsp. bulgaricus, was spread by a root carrier in an office housing more than 20 participants undertaking normal activities, and the microbiotas on skin and environmental surfaces were analyzed before and after invasion. First, we found that the invader was trackable. Its identity and emission source could be determined using microbial-interaction networks, and the root carrier could be identified using a rank analysis. Without prior information, L. bulgaricus could be identified as the invader emitted from a source that exclusively contained the invader, and the probable root carrier could be located. In addition to the single-taxon invasion by L. bulgaricus, multiple-taxon invasion was observed, as genera from sputum/saliva exhibited co-occurrence relationships on skin and environmental surfaces. Second, the invader had a below-neutral distribution in a neutral community model, suggesting that hands accrued heavier invader contamination than environmental surfaces. Third, a proximity effect was observed on a surface touch network. Invader contamination on surfaces decreased with increasing geodesic distance from the hands of the carrier, indicating that the carrier’s touching behaviors were the main driver of fomite transmission. Taken together, these results demonstrate the invasion ecology principles in fomite transmission and provide a general basis for the management of ecological fomite transmission. IMPORTANCE Fomite transmission contributes to the spread of many infectious diseases. However, pathogens in fomite transmission typically are either investigated individually without considering the context of native microbiotas or investigated in a nondiscriminatory way from the dispersal of microbiotas. In this study, we adopted an invasion ecology framework in which we considered pathogens as invaders, the surface environment as an ecosystem, and human behaviors as the driver of microbial dispersal. With this approach, we assessed the ability of quantitative ecological theories to track and forecast pathogen movements in fomite transmission. By uncovering the relationships between the invader and native microbiotas and between human behaviors and invader/microbiota dispersal, we demonstrated that fomite transmission follows idiosyncratic invasion ecology principles. Our findings suggest that attempts to manage fomite transmission for public health purposes should focus on the microbial communities and anthropogenic factors involved, in addition to the pathogens.
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spelling pubmed-92384042022-06-29 Fomite Transmission Follows Invasion Ecology Principles Wang, Peihua Tong, Xinzhao Zhang, Nan Miao, Te Chan, Jack P. T. Huang, Hong Lee, Patrick K. H. Li, Yuguo mSystems Research Article The invasion ecology principles illustrated in many ecosystems have not yet been explored in the context of fomite transmission. We hypothesized that invaders in fomite transmission are trackable, are neutrally distributed between hands and environmental surfaces, and exhibit a proximity effect. To test this hypothesis, a surrogate invader, Lactobacillus delbrueckii subsp. bulgaricus, was spread by a root carrier in an office housing more than 20 participants undertaking normal activities, and the microbiotas on skin and environmental surfaces were analyzed before and after invasion. First, we found that the invader was trackable. Its identity and emission source could be determined using microbial-interaction networks, and the root carrier could be identified using a rank analysis. Without prior information, L. bulgaricus could be identified as the invader emitted from a source that exclusively contained the invader, and the probable root carrier could be located. In addition to the single-taxon invasion by L. bulgaricus, multiple-taxon invasion was observed, as genera from sputum/saliva exhibited co-occurrence relationships on skin and environmental surfaces. Second, the invader had a below-neutral distribution in a neutral community model, suggesting that hands accrued heavier invader contamination than environmental surfaces. Third, a proximity effect was observed on a surface touch network. Invader contamination on surfaces decreased with increasing geodesic distance from the hands of the carrier, indicating that the carrier’s touching behaviors were the main driver of fomite transmission. Taken together, these results demonstrate the invasion ecology principles in fomite transmission and provide a general basis for the management of ecological fomite transmission. IMPORTANCE Fomite transmission contributes to the spread of many infectious diseases. However, pathogens in fomite transmission typically are either investigated individually without considering the context of native microbiotas or investigated in a nondiscriminatory way from the dispersal of microbiotas. In this study, we adopted an invasion ecology framework in which we considered pathogens as invaders, the surface environment as an ecosystem, and human behaviors as the driver of microbial dispersal. With this approach, we assessed the ability of quantitative ecological theories to track and forecast pathogen movements in fomite transmission. By uncovering the relationships between the invader and native microbiotas and between human behaviors and invader/microbiota dispersal, we demonstrated that fomite transmission follows idiosyncratic invasion ecology principles. Our findings suggest that attempts to manage fomite transmission for public health purposes should focus on the microbial communities and anthropogenic factors involved, in addition to the pathogens. American Society for Microbiology 2022-05-03 /pmc/articles/PMC9238404/ /pubmed/35502902 http://dx.doi.org/10.1128/msystems.00211-22 Text en Copyright © 2022 Wang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Wang, Peihua
Tong, Xinzhao
Zhang, Nan
Miao, Te
Chan, Jack P. T.
Huang, Hong
Lee, Patrick K. H.
Li, Yuguo
Fomite Transmission Follows Invasion Ecology Principles
title Fomite Transmission Follows Invasion Ecology Principles
title_full Fomite Transmission Follows Invasion Ecology Principles
title_fullStr Fomite Transmission Follows Invasion Ecology Principles
title_full_unstemmed Fomite Transmission Follows Invasion Ecology Principles
title_short Fomite Transmission Follows Invasion Ecology Principles
title_sort fomite transmission follows invasion ecology principles
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9238404/
https://www.ncbi.nlm.nih.gov/pubmed/35502902
http://dx.doi.org/10.1128/msystems.00211-22
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