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A Nationwide Genomic Study of Clinical Klebsiella Pneumoniae in Norway

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A Nationwide Genomic Study of Clinical Klebsiella Pneumoniae in Norway bioRxiv preprint doi: https://doi.org/10.1101/2021.07.16.452602; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 A nationwide genomic study of clinical Klebsiella pneumoniae in 2 Norway 2001-2015: Introduction and spread of ESBL facilitated by 3 CG15 and CG307 4 5 Aasmund Fostervold1,2, Marit A.K. Hetland1,3, Ragna Bakksjø1, Eva Bernhoff1, Kathryn E Holt4,5, Ørjan 6 Samuelsen6,7, Gunnar Skov Simonsen8,9, Arnfinn Sundsfjord6,9, Kelly L Wyres4, Iren H. Løhr1, The 7 Norwegian Study Group on Klebsiella pneumoniae 8 Affiliations: 9 1. Department of Medical Microbiology, Stavanger University Hospital, Stavanger, Norway 10 2. Department of Clinical Science, Faculty of Medicine, University of Bergen, Bergen, Norway 11 3. Department of Biological Sciences, Faculty of Mathematics and Natural Sciences, University of 12 Bergen, Bergen, Norway 13 4. Department of Infectious Diseases, Central Clinical School, Monash University, Melbourne, 14 Australia 15 5. Department of Infection Biology, London School of Hygiene and Tropical Medicine, London, UK 16 6. Norwegian National Advisory Unit on Detection of Antimicrobial Resistance, University Hospital of 17 North Norway, Tromsø, Norway 18 7. Department of Pharmacy, Faculty of Health Sciences, UiT The Arctic University of Norway, Tromsø, 19 Norway 20 8. Department of Medical Biology, Faculty of Health Sciences, UiT The Arctic University of Norway, 21 Tromsø, Norway 22 9. Department of Microbiology and Infection Control, University Hospital of North-Norway, Tromsø, 23 Norway 24 25 Collaborators: 26 The Norwegian Study Group on Klebsiella pneumoniae: bioRxiv preprint doi: https://doi.org/10.1101/2021.07.16.452602; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 27 Ståle Tofteland, Paul C. Lindemann, Nina Handal, Åshild M. Rødland, Aleksandra Jakovljev, Sandra 28 Åsheim, Karianne W. Gammelsrud, Rolf A. Sandnes, Einar Weme, Angela Kümmel, Einar Nilsen, 29 Belinda L. Lindstad, Anne Hollekim, Reidar Hjetland, Anne R. Oseid, Liv Jorunn Hafne 30 31 Corresponding author: 32 Aasmund Fostervold 33 Avdeling for medisinsk mikrobiologi 34 Stavanger Universitetssykehus HF 35 Postboks 8100 36 4068 Stavanger 37 NORWAY 38 Phone: +47 51518800 39 Email: [email protected] 40 41 Running title: 42 Genomic study of clinical Klebsiella pneumoniae in Norway 2001-2015 43 bioRxiv preprint doi: https://doi.org/10.1101/2021.07.16.452602; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 44 Synopsis 45 46 Objective 47 We have used the nationwide Norwegian surveillance program on resistant microbes in humans 48 (NORM) to address longitudinal changes in the population structure K. pneumoniae isolates during 49 2001-15, encompassing the emergence and spread of ESBL-producing Enterobacterales (ESBL-E) in 50 Norway. 51 Material and methods 52 Among blood (n= 6124) and urinary tract (n=5496) surveillance isolates from 2001-15, we used 53 Illumina technology to whole genome sequence 201 ESBL-producing isolates from blood (n=130) and 54 urine (n=71), and 667 non-ESBL isolates from blood. Complete genomes for four isolates were 55 resolved with Oxford Nanopore sequencing. 56 Results 57 In a highly diverse collection, Klebsiella variicola ssp. variicola caused a quarter of Klebsiella 58 pneumoniae species complex bacteraemias. ESBL-production was limited to K. pneumoniae sensu 59 stricto (98.5 %). A diverse ESBL population of 57 clonal groups (CGs) were dominated by multidrug 60 resistant CG307 (17%), CG15 (12%), CG70 (6%), CG258 (5%) and CG45 (5%) carrying blaCTX-M-15. 61 Yersiniabactin was significantly more common in ESBL-positive (37.8%) compared to non-ESBL K. 62 pneumoniae sensu stricto isolates (12.7%), indicating convergence of virulence and resistance 63 determinants 64 65 Moreover, we found a significant lower prevalence of yersinabactin (3.0 %, 37.8 % and 17.3 %), 66 IncFIB (58.7 %, 87.9 % and 79.4 %) and IncFII plasmid replicons (40.5 %, 82.8 % and 54.2%) in K. 67 variicola ssp. variicola compared to ESBL- and non-ESBL K. pneumoniae sensu stricto, respectively. bioRxiv preprint doi: https://doi.org/10.1101/2021.07.16.452602; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 68 Conclusion 69 The increase in Norwegian KpSC ESBLs during 2010-15 was driven by blaCTX-M-15 carrying CG307 and 70 CG15. K. variicola ssp. variicola was a frequent cause of invasive KpSC infection, but rarely carried 71 ESBL. 72 73 Introduction 74 Klebsiella pneumoniae is an important human pathogen 1 and acknowledged as a key host for the 75 spread of antimicrobial resistance (AMR)2, 3. The global spread of multidrug resistance (MDR) 4 K. 76 pneumoniae is closely linked to the spread of extended-spectrum β-lactamases (ESBLs) and 77 carbapenemases. This has been facilitated by successful clonal lineages or clonal groups (CGs) such as 78 CG258, CG15 and CG307 5-7, and horizontal gene transfer (HGT) 2, 8, fueled by antibiotic selection 9. 79 Whilst K. pneumoniae typically causes severe infections in vulnerable hospitalized patients 1, some 80 hypervirulent (HV) clones cause community acquired invasive infections, often in healthy individuals 81 10. HV-clones cluster in CG23, CG65 and CG86, and harbour capsular loci K1 or K2, siderophores and 82 other virulence factors supporting colonization, tissue invasion and immune evasion 10, 11. High-risk K. 83 pneumoniae clones, categorized as either MDR or HV, rarely display both traits 12. However, in recent 84 years, convergence of the two traits has been reported 13. 85 86 K. pneumoniae is a highly diverse species, and the term K. pneumoniae species complex (KpSC) has 87 been introduced to encompass seven closely related taxa 14, of which K. pneumoniae sensu stricto, 88 Klebsiella variicola and Klebsiella quasipneumoniae are the most frequently reported in human 89 clinical samples 15, 16. bioRxiv preprint doi: https://doi.org/10.1101/2021.07.16.452602; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 90 Most molecular epidemiological studies of KpSC have focused on outbreaks or isolates with 91 particular characteristics such as AMR or virulence, most often with a cross-sectional study design. 92 Thus, there is a need for longitudinal studies, including both resistant and susceptible isolates, to 93 improve our understanding of the population dynamics in clinical KpSC isolates. 94 Here, we have used the Norwegian surveillance program on resistant microbes (NORM) during 2001- 95 2015 to address the longitudinal dynamics of KpSC clinical isolates, dominant CGs and their 96 associations with clinically important AMR- and virulence determinants. 97 The nationwide data show that the emergence of ESBL-producing KpSC clinical isolates in Norway has 98 been dominated by MDR blaCTX-M-15 carrying K. pneumoniae sensu stricto, with CG15 and CG307 as 99 major lineages. K. variicola ssp. variicola is a significant contributor to KpSC bacteraemias, but rarely 100 carries ESBL genes in this geographical setting. 101 102 Material and methods 103 Bacterial isolates 104 NORM monitors AMR in Klebsiella spp. isolated from blood and urine isolates. Antimicrobial 105 susceptibility is performed and interpreted according to EUCAST guidelines and breakpoints 17. 106 Isolates with reduced susceptibility to cefotaxime and/or ceftazidime are categorized as ESBL or non- 107 ESBL based on phenotypical ESBL-testing 18. Isolates are stored locally at -80°C at the participating 108 laboratories 18. 109 All putative ESBL-producing KpSC blood (n=149) and urine isolates (n=91) from 2001-2015 registered 110 in the NORM database were included in the study. For comparison, a subset of non-ESBL blood 111 culture isolates (n=815) were included. To achieve a balanced sample for each year and to maintain a 112 representative geographical and temporal distribution, consecutive entries were selected from each bioRxiv preprint doi: https://doi.org/10.1101/2021.07.16.452602; this version posted July 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 113 laboratory according to the following key: 2001, all isolates; 2005, every 2 out of 3; 2009, every 1 out 114 of 2; and 2015, every 1 out of 3 (Figure S1). 115 116 Isolates registered as either K. pneumoniae or Klebsiella spp. were included. Species identification 117 was confirmed by MALDI-TOF MS (MBT Compass Library DB-6903, Bruker Daltonik), and 118 subsequently by whole genome sequencing. Only KpSC isolates were included for further analyses. 119 Antimicrobial susceptibility profiles, laboratory, year and source of isolation were retrieved from the 120 NORM database. For isolates with discordant ESBL geno- and phenotype, the phenotype was 121 confirmed using the combined disc method (Becton Dickinson, New Jersey, USA) 19.
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