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Axel Janssen Mechanisms and Evolution of Colistin Resistance in Clinical Enterobacteriaceae

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Axel Janssen Mechanisms and Evolution of Colistin Resistance in Clinical Enterobacteriaceae Mechanisms and evolution of colistin resistance in clinical Enterobacteriaceae Axel Janssen Mechanisms and evolution of colistin resistance in clinical Enterobacteriaceae Axel B. Janssen Mechanisms and evolution of colistin resistance in clinical Enterobacteriaceae PhD thesis, Utrecht University, Utrecht, the Netherlands Author: Axel B. Janssen Cover design: Axel B. Janssen Lay-out: Axel B. Janssen Printing: ProefschriftMaken ISBN: 978-94-6380-950-4 © Axel B. Janssen, 2020, Utrecht, the Netherlands. All rights reserved. No parts of this thesis may be reproduced, stored in a retrieval system, or transmitted in any form or by any means without prior permission of the author. The copyright of articles that have been published has been transferred to the respective journals. Printing of this thesis was financially supported by: the Netherlands Society of Medical Microbiology, the Royal Netherlands Society for Microbiology, Infection & Immunity Utrecht, and the University Medical Center Utrecht. Mechanisms and evolution of colistin resistance in clinical Enterobacteriaceae Mechanismen en evolutie van colistin resistentie in klinische Enterobacteriaceae (met een samenvatting in het Nederlands) Proefschrift ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector magnificus, prof. dr. H.R.B.M. Kummeling, ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op dinsdag 3 november 2020 des middags te 12.45 uur door Absalom Benjamin Janssen geboren op 31 oktober 1991 te Nijmegen Promotoren: Prof. dr. R.J.L. Willems Prof. dr. ir. W. van Schaik Beoordelingscommissie: Prof. dr. J.A.J.W. Kluytmans Prof. dr. S.H.M. Rooijakkers Prof. dr. J.W.A. Rossen Prof. dr. J.P.M. Tommassen Dr. ir. M.G.J. de Vos Paranimfen: Dr. T.P. Praest Ing. M. Salomons Table of contents Chapter 1 General introduction 8 Chapter 2 Nonclonal emergence of colistin resistance associated 34 with mutations in the BasRS two-component system in Escherichia coli bloodstream isolates Chapter 3 Microevolution of acquired colistin resistance in 66 Enterobacteriaceae isolated from ICU patients receiving selective decontamination of the digestive tract Chapter 4 Genomic characterization of colistin heteroresistance in 98 Klebsiella pneumoniae during a nosocomial outbreak Chapter 5 In vitro evolution of colistin resistance in the 124 Klebsiella pneumoniae complex follows multiple evolutionary trajectories with variable effects on fitness and virulence characteristics Chapter 6 General discussion 170 Closing Nederlandse samenvatting (Dutch summary) 188 pages Acknowledgements List of publications About the author Chapter 1 General introduction Axel B. Janssen Chapter 1 Escherichia coli and Klebsiella pneumoniae as multidrug‑resistant Gram‑negative opportunistic pathogens 1 Escherichia coli and Klebsiella pneumoniae are facultative anaerobic, rod‑shaped, Gram‑negative opportunistic pathogens in the Enterobacteriaceae family, and are asymptomatic colonizers of the intestinal microbiota (1–3). In addition, K. pneumoniae also asymptotically colonizes the skin, and the upper respiratory tract. E. coli and K. pneumoniae are frequently observed pathogens, that can cause infections outside of their respective niches. Common opportunistic infections caused by both E. coli and K. pneumoniae are bloodstream, and urinary tract infections (4–7). Individually, E. coli is well known to cause enteric infections (1, 5), whilst K. pneumoniae may also cause soft tissue infections, and pneumonia (2, 8). K. pneumoniae, together with Enterococcus faecium, Staphylococcus aureus, Acinetobacter baumannii, Pseudomonas aeruginosa, and species from the Enterobacter genus, is a member of the group of ESKAPE pathogens (9). Together, like the acronym of their genus names suggests, they are known for their ability to evade the effects of antibiotic treatments in patients, through various mechanisms of antibiotic resistance. Due to the increasing rate of antibiotic resistance, it has been suggested to include E. coli in this group; forming the ESKAPEE pathogens (10). The rate of antibiotic resistance in both E. coli and K. pneumoniae has increased all over the world, over the last two decades (11, 12). Both species have become increasingly resistant to multiple types of antibiotics, including fluoroquinolones, third‑generation cephalosporins, and aminoglycosides (5, 11, 13, 14). Through the spread of carbapenemases located on mobile genetic elements, K. pneumoniae has also increasingly acquired carbapenem resistance (5, 11, 13–16). Some countries report sporadic outbreaks of carbapenem‑resistant K. pneumoniae, but other countries suffer from endemic presence these types of resistant K. pneumoniae (5, 16). Thus, the prevalence of carbapenem resistance in K. pneumoniae varies greatly between countries. Within the European Union, the rate of carbapenem resistance in invasive K. pneumoniae isolates has been determined to vary between 0% and 64% between countries. Within carbapenem‑resistant K. pneumoniae, the rate of resistance against colistin in carbapenem‑resistant K. pneumoniae has been estimated at 28% (17). In contrast to K. pneumoniae, the rate of carbapenem resistance in invasive E. coli isolates is lower, with 0‑2% of isolates reported as resistant, depending on the individual country (13, 18). A notable point in the increasing number of infections caused by multidrug‑resistant E. coli and K. pneumoniae is the spread of particularly multidrug‑resistant lineages. Within E. coli, the ST131 lineage is known for its ability to cause extra‑intestinal infections (1). Within the ST131 lineage, the C clade 10 General introduction is particularly well‑known for its multidrug‑resistant nature, with the acquisition of CTX‑M class extended‑spectrum ß‑lactamases, making this group resistant to third‑generation cephalosporins. Furthermore, clade C ST131 E. coli strains have 1 also acquired fluoroquinolone resistance through point mutations in DNA gyrase and DNA topoisomerase genes (19, 20). Within K. pneumoniae, the ST15, ST147, ST258, and ST395 are well known multidrug‑resistant lineages. These lineages can harbour CTX‑M class extended‑spectrum ß‑lactamases, but also NDM‑type, or OXA‑48‑type carbapenemases (21–23). Some of these multidrug‑resistant E. coli and K. pneumoniae lineages are also particularly well‑equipped to cause infections through the acquisition of virulence factors on the mobile genetic elements that can encode the antibiotic resistance genes (24). The increasing rate of multidrug resistance, including carbapenem resistance in Enterobacteriaceae and other types of Gram‑negative bacteria, has led to a revival in the use of colistin as a last‑resort drug to treat infections with these opportunistic pathogens (25). In some countries, failures in hospital hygiene measures has lead an endemic spread of carbapenem‑resistant K. pneumoniae lineages. In these countries, this spread has led to an particular increase in the use of colistin in order to treat infections with these pathogens (26, 27). However, as the use of colistin has increased, outbreaks with carbapenem‑resistant, but also colistin‑resistant K. pneumoniae in clinical settings are increasingly frequent (23, 28–31). The increasing prevalence of Enterobacteriaceae that are resistant to both carbapenems, and colistin, is of growing concern for public health. Colistin: a Gram‑negative selective antibiotic Colistin belongs to the polymyxin class of antibiotics. Polymyxin antibiotics were first isolated from Paenibacillus polymyxa in 1947 and were first used in clinical settings in the 1950s (32). Polymyxins are amphipathic, non‑ribosomally synthesized, cyclic lipopeptides, composed of a decapeptide with an intramolecular heptapeptide loop, and an N‑terminal fatty acid group (Figure 1A). A number of different polymyxins have been described, varying in their exact composition of amino acids in the peptide portion, and fatty acid group (32). From the ten amino acids, those in positions 3, 6, 7, and 10 may vary. The fatty acid group may vary from a seven‑ to a nine‑carbon fatty acid, and may be methylated, hydroxylated, or sulphonated (32–34). Although there is variation in the exact composition of the each polymyxin, the amphipathic structure of polymyxins is conserved. The hydrophobic aspects of polymyxins is conserved in both the fatty acid group, and the hydrophobic 11 Chapter 1 characteristics of the variable amino acids in position 6 and 7 (Figure 1A) (32, 34). The hydrophilic nature is conserved in the polar residue of threonine at position 1 2, the cationic residues of the L‑α,γ‑diaminobutyric acid (Dab) groups in positions 1, 5, 8, and 9, and the conserved hydrophilic characteristics of the variable amino acids in positions 3 and 10 (32, 34). These hydrophobic and hydrophilic traits of the polymyxin molecule allow the molecule to fold into an amphipathic structure. This characteristic is crucial to the mechanism of action of polymyxins. Since colistin is the most widely used polymyxin, and because all polymyxins have similar characteristics, we have used colistin as a representative for the polymyxin class of antibiotics in the rest of this thesis (32, 33). Figure 1: Chemical structure of polymyxins and colistin. A) General chemical structure of polymyxins. Polymyxins are composed of a non‑ribosomally synthesized decapaptide (amino acids are number 1 through 10) with an intramolecular loop (amino acids 4 through 10), linked to a fatty acid (FA) (32). The fatty acid may differ between
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