Genomic insights into the emergence and spread of antimicrobial-resistant bacterial pathogens

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Abstract

Whole-genome sequencing (WGS) has been vital for revealing the rapid temporal and spatial evolution of antimicrobial resistance (AMR) in bacterial pathogens. Some antimicrobialresistant pathogens have outpaced us, with untreatable infections appearing in hospitals and the community. However,WGS has additionally provided us with enough knowledge to initiate countermeasures. Although we cannot stop bacterial adaptation, the predictability of many evolutionary processes in AMR bacteria offers us an opportunity to channel them using new control strategies. Furthermore, by usingWGS for coordinating surveillance and to create a more fundamental understanding of the outcome of antimicrobial treatment and AMR mechanisms, we can use current and future antimicrobials more effectively and aim to extend their longevity.

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Most cited references 23

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Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future.

Magnus Unemo, William M Shafer (2014)

Neisseria gonorrhoeae is evolving into a superbug with resistance to previously and currently recommended antimicrobials for treatment of gonorrhea, which is a major public health concern globally. Given the global nature of gonorrhea, the high rate of usage of antimicrobials, suboptimal control and monitoring of antimicrobial resistance (AMR) and treatment failures, slow update of treatment guidelines in most geographical settings, and the extraordinary capacity of the gonococci to develop and retain AMR, it is likely that the global problem of gonococcal AMR will worsen in the foreseeable future and that the severe complications of gonorrhea will emerge as a silent epidemic. By understanding the evolution, emergence, and spread of AMR in N. gonorrhoeae, including its molecular and phenotypic mechanisms, resistance to antimicrobials used clinically can be anticipated, future methods for genetic testing for AMR might permit region-specific and tailor-made antimicrobial therapy, and the design of novel antimicrobials to circumvent the resistance problems can be undertaken more rationally. This review focuses on the history and evolution of gonorrhea treatment regimens and emerging resistance to them, on genetic and phenotypic determinants of gonococcal resistance to previously and currently recommended antimicrobials, including biological costs or benefits; and on crucial actions and future advances necessary to detect and treat resistant gonococcal strains and, ultimately, retain gonorrhea as a treatable infection. Copyright © 2014, American Society for Microbiology. All Rights Reserved.

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Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe

Kathryn E. Holt, Stephen Baker, François-Xavier Weill … (2012)

Shigella are human-adapted Escherichia coli that have gained the ability to invade the human gut mucosa and cause dysentery 1,2 , spreading efficiently via low-dose fecal-oral transmission 3,4 . Historically, S. sonnei has been predominantly responsible for dysentery in developed countries, but is now emerging as a problem in the developing world, apparently replacing the more diverse S. flexneri in areas undergoing economic development and improvements in water quality 4-6 . Classical approaches have shown S. sonnei is genetically conserved and clonal 7 . We report here whole-genome sequencing of 132 globally-distributed isolates. Our phylogenetic analysis shows that the current S. sonnei population descends from a common ancestor that existed less than 500 years ago and has diversified into several distinct lineages with unique characteristics. Our analysis suggests the majority of this diversification occurred in Europe, followed by more recent establishment of local pathogen populations in other continents predominantly due to the pandemic spread of a single, rapidly-evolving, multidrug resistant lineage.

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Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts.

A. E. MATHER, S W J Reid, D. J. Maskell … (2013)

The global epidemic of multidrug-resistant Salmonella Typhimurium DT104 provides an important example, both in terms of the agent and its resistance, of a widely disseminated zoonotic pathogen. Here, with an unprecedented national collection of isolates collected contemporaneously from humans and animals and including a sample of internationally derived isolates, we have used whole-genome sequencing to dissect the phylogenetic associations of the bacterium and its antimicrobial resistance genes through the course of an epidemic. Contrary to current tenets supporting a single homogeneous epidemic, we demonstrate that the bacterium and its resistance genes were largely maintained within animal and human populations separately and that there was limited transmission, in either direction. We also show considerable variation in the resistance profiles, in contrast to the largely stable bacterial core genome, which emphasizes the critical importance of integrated genotypic data sets in understanding the ecology of bacterial zoonoses and antimicrobial resistance.

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Author and article information

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Journal ID (nlm-ta): Science

Journal ID (iso-abbrev): Science

Journal ID (publisher-id): Science

Title: Science (New York, N.y.)

Publisher: American Association for the Advancement of Science

ISSN (Print): 0036-8075

ISSN (Electronic): 1095-9203

Publication date (Electronic): 18 May 2018

Publication date (Print): 2017

Volume: 360

Issue: 6390

Pages: 733-738

Affiliations

[1 ]Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam

[2 ]Centre for Tropical Medicine and Global Health, Oxford University, Oxford, UK

[3 ]The Department of Medicine, University of Cambridge, Cambridge, UK

[4 ]The Wellcome Trust Sanger Institute, Cambridge, UK

[5 ]The London School of Hygiene and Tropical Medicine, London, UK

[6 ]Institut Pasteur, Paris, France

[7 ]Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria, Australia

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[* ]Corresponding author. Email: sbaker@ 123456oucru.org

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Publisher ID: Science-360-733

DOI: 10.1126/science.aar3777

PMC ID: 6510332

PubMed ID: 29773743

SO-VID: c4e4bafa-2892-4fbb-97be-099b124656eb

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Genomic insights into the emergence and spread of antimicrobial-resistant bacterial pathogens

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Most cited references 23

Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future.

Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe

Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts.

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