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Volume 10, Issue 11

Longitudinal genomic surveillance of a UK intensive care unit shows a lack of patient colonisation by multi-drug-resistant Gram-negative bacterial pathogens Open Access

Abstract

Vulnerable patients in an intensive care unit (ICU) setting are at high risk of infection from bacteria including gut-colonising and species. Complex ICU procedures often depend on successful antimicrobial treatment, underscoring the importance of understanding the extent of patient colonisation by multi-drug-resistant organisms (MDROs) in large UK ICUs. Previous work on ICUs globally uncovered high rates of colonisation by transmission of MDROs, but the situation in UK ICUs is less understood. Here, we investigated the diversity and antibiotic resistance gene (ARG) carriage of bacteria present in one of the largest UK ICUs at the Queen Elizabeth Hospital Birmingham (QEHB), focusing primarily on as both a widespread commensal and a globally disseminated multi-drug-resistant pathogen. Samples were taken during highly restrictive coronavirus disease 2019 (COVID-19) control measures from May to December 2021. Whole-genome and metagenomic sequencing were used to detect and report strain-level colonisation of patients, focusing on sequence types (STs), their colonisation dynamics and antimicrobial resistance gene carriage. We found a lack of multi-drug resistance (MDR) in the QEHB. Only one carbapenemase-producing organism was isolated, a carrying . There was no evidence supporting the spread of this strain, and there was little evidence overall of nosocomial acquisition or circulation of colonising . Whilst 22 different STs were identified, only 1 strain of the pandemic ST131 lineage was isolated. This ST131 strain was non-MDR and was found to be a clade A strain, associated with low levels of antibiotic resistance. Overall, the QEHB ICU had very low levels of pandemic or MDR strains, a result that may be influenced in part by the strict COVID-19 control measures in place at the time. Employing some of these infection prevention and control measures where reasonable in all ICUs might therefore assist in maintaining low levels of nosocomial MDR.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): AMR , E. coli and ICU
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-11-04
2024-12-02
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References

  1. O’Neill J. The review on antimicrobial resistance - antimicrobial resistance:tackling a crisis for the health and wealth of nations; 2014
  2. Vincent J-L, Sakr Y, Singer M, Martin-Loeches I, Machado FR et al. Prevalence and outcomes of infection among patients in Intensive Care Units in 2017. JAMA 2020; 323:1478–1487 [View Article] [PubMed]
     [Google Scholar]
  3. Kaper JB. Pathogenic Escherichia coli. Int J Med Microbiol 2005; 295:355–356 [View Article] [PubMed]
     [Google Scholar]
  4. Paczosa MK, Mecsas J. Klebsiella pneumoniae: going on the offense with a strong defense. Microbiol Mol Biol Rev 2016; 80:629–661 [View Article] [PubMed]
     [Google Scholar]
  5. Hu Y, Zhang H, Wei L, Feng Y, Wen H et al. Competitive transmission of carbapenem-resistant Klebsiella pneumoniae in a newly opened intensive care unit. mSystems 2022; 7:e0079922 [View Article] [PubMed]
     [Google Scholar]
  6. Moran RA, Baomo L, Doughty EL, Guo Y, Ba X et al. Extended-spectrum β-lactamase genes traverse the Escherichia coli populations of intensive care unit patients, staff, and environment. Microbiol Spectr 2023; 11:e0507422 [View Article] [PubMed]
     [Google Scholar]
  7. Wei L, Wu L, Wen H, Feng Y, Zhu S et al. Spread of carbapenem-resistant Klebsiella pneumoniae in an intensive care unit: a whole-genome sequence-based prospective observational study. Microbiol Spectr 2021; 9:e0005821 [View Article] [PubMed]
     [Google Scholar]
  8. Zong Z, Fenn S, Connor C, Feng Y, McNally A. Complete genomic characterization of two Escherichia coli lineages responsible for a cluster of carbapenem-resistant infections in a Chinese hospital. J Antimicrob Chemother 2018; 73:2340–2346 [View Article] [PubMed]
     [Google Scholar]
  9. Doughty EL, Liu H, Moran RA, Hua X, Ba X et al. Endemicity and diversification of carbapenem-resistant Acinetobacter baumannii in an intensive care unit. Lancet Reg Health West Pac 2023; 37:100780 [View Article] [PubMed]
     [Google Scholar]
  10. Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MCJ, van Genderen PJJ et al. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis 2017; 17:78–85 [View Article] [PubMed]
     [Google Scholar]
  11. Kantele A, Kuenzli E, Dunn SJ, Dance DAB, Newton PN et al. Dynamics of intestinal multidrug-resistant bacteria colonisation contracted by visitors to a high-endemic setting: a prospective, daily, real-time sampling study. Lancet Microbe 2021; 2:e151–e158 [View Article] [PubMed]
     [Google Scholar]
  12. Blot S, Ruppé E, Harbarth S, Asehnoune K, Poulakou G et al. Healthcare-associated infections in adult intensive care unit patients: changes in epidemiology, diagnosis, prevention and contributions of new technologies. Intensive Crit Care Nurs 2022; 70:103227 [View Article] [PubMed]
     [Google Scholar]
  13. De Waele JJ, Akova M, Antonelli M, Canton R, Carlet J et al. Antimicrobial resistance and antibiotic stewardship programs in the ICU: insistence and persistence in the fight against resistance. A position statement from ESICM/ESCMID/WAAAR round table on multi-drug resistance. Intensive Care Med 2018; 44:189–196 [View Article] [PubMed]
     [Google Scholar]
  14. Ali M, Naureen H, Tariq MH, Farrukh MJ, Usman A et al. Rational use of antibiotics in an intensive care unit: a retrospective study of the impact on clinical outcomes and mortality rate. Infect Drug Resist 2019; 12:493–499 [View Article] [PubMed]
     [Google Scholar]
  15. Ravi A, Halstead FD, Bamford A, Casey A, Thomson NM et al. Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients. Microb Genom 2019; 5:e000293 [View Article] [PubMed]
     [Google Scholar]
  16. Ayobami O, Willrich N, Harder T, Okeke IN, Eckmanns T et al. The incidence and prevalence of hospital-acquired (carbapenem-resistant) Acinetobacter baumannii in Europe, Eastern Mediterranean and Africa: a systematic review and meta-analysis. Emerg Microbes Infect 2019; 8:1747–1759 [View Article] [PubMed]
     [Google Scholar]
  17. Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Health 2015; 109:309–318 [View Article] [PubMed]
     [Google Scholar]
  18. Agency UHS. English Surveillance Programme for Antimicrobial Utilisation and Resistance (ESPAUR) Report 2021 to 2022 London: UK Health Security Agency; 2022
     [Google Scholar]
  19. Godijk NG, Bootsma MCJ, Bonten MJM. Transmission routes of antibiotic resistant bacteria: a systematic review. BMC Infect Dis 2022; 22:482 [View Article] [PubMed]
     [Google Scholar]
  20. Filius PMG, Gyssens IC, Kershof IM, Roovers PJE, Ott A et al. Colonization and resistance dynamics of gram-negative bacteria in patients during and after hospitalization. Antimicrob Agents Chemother 2005; 49:2879–2886 [View Article] [PubMed]
     [Google Scholar]
  21. Lee SY, Kotapati S, Kuti JL, Nightingale CH, Nicolau DP. Impact of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella species on clinical outcomes and hospital costs: a matched cohort study. Infect Control Hosp Epidemiol 2006; 27:1226–1232 [View Article] [PubMed]
     [Google Scholar]
  22. Lambert M-L, Suetens C, Savey A, Palomar M, Hiesmayr M et al. Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study. Lancet Infect Dis 2011; 11:30–38 [View Article] [PubMed]
     [Google Scholar]
  23. McDonald D, Ackermann G, Khailova L, Baird C, Heyland D et al. Extreme dysbiosis of the microbiome in critical illness. mSphere 2016; 1:e00199-16 [View Article] [PubMed]
     [Google Scholar]
  24. Wischmeyer PE, McDonald D, Knight R. Role of the microbiome, probiotics, and “dysbiosis therapy” in critical illness. Curr Opin Crit Care 2016; 22:347–353 [View Article] [PubMed]
     [Google Scholar]
  25. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article] [PubMed]
     [Google Scholar]
  26. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  27. Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom 2018; 4:e000192 [View Article] [PubMed]
     [Google Scholar]
  28. Lam MMC, Wick RR, Watts SC, Cerdeira LT, Wyres KL et al. A genomic surveillance framework and genotyping tool for Klebsiella pneumoniae and its related species complex. Nat Commun 2021; 12:4188 [View Article] [PubMed]
     [Google Scholar]
  29. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
     [Google Scholar]
  30. Carattoli A, Hasman H. PlasmidFinder and In Silico pMLST: identification and typing of plasmid replicons in Whole-Genome Sequencing (WGS). Methods Mol Biol 2020; 2075:285–294 [View Article] [PubMed]
     [Google Scholar]
  31. Liu B, Zheng D, Zhou S, Chen L, Yang J. VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res 2022; 50:D912–D917 [View Article] [PubMed]
     [Google Scholar]
  32. Kaminski J, Gibson MK, Franzosa EA, Segata N, Dantas G et al. High-specificity targeted functional profiling in microbial communities with ShortBRED. PLoS Comput Biol 2015; 11:e1004557 [View Article] [PubMed]
     [Google Scholar]
  33. Alcock BP, Huynh W, Chalil R, Smith KW, Raphenya AR et al. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database. Nucleic Acids Res 2023; 51:D690–D699 [View Article] [PubMed]
     [Google Scholar]
  34. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:e000131 [View Article] [PubMed]
     [Google Scholar]
  35. Cerceo E, Deitelzweig SB, Sherman BM, Amin AN. Multidrug-resistant gram-negative bacterial infections in the hospital setting: overview, implications for clinical practice, and emerging treatment options. Microb Drug Resist 2016; 22:412–431 [View Article] [PubMed]
     [Google Scholar]
  36. Snaith AE, Dunn SJ, Moran RA, Newton PN, Dance DAB et al. The highly diverse plasmid population found in Escherichia coli colonizing travellers to Laos and its role in antimicrobial resistance gene carriage. Microb Genom 2023; 9:mgen001000 [View Article] [PubMed]
     [Google Scholar]
  37. Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 2018; 31:e00088-17 [View Article] [PubMed]
     [Google Scholar]
  38. Moran RA, Behruznia M, Holden E, Garvey MI, McNally A. PQEB1: a hospital outbreak plasmid lineage carrying blakpc-2. bioRxiv 2024 [View Article]
     [Google Scholar]
  39. Ludden C, Coll F, Gouliouris T, Restif O, Blane B et al. Defining nosocomial transmission of Escherichia coli and antimicrobial resistance genes: a genomic surveillance study. Lancet Microbe 2021; 2:e472–e480 [View Article] [PubMed]
     [Google Scholar]
  40. Mills EG, Martin MJ, Luo TL, Ong AC, Maybank R et al. A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network. Genome Med 2022; 14:147 [View Article] [PubMed]
     [Google Scholar]
  41. Roberts LW, Hoi LT, Khokhar FA, Hoa NT, Giang TV et al. Genomic characterisation of multidrug-resistant Escherichia coli, Klebsiella pneumoniae, and Acinetobacter baumannii in two intensive care units in Hanoi, Viet Nam: a prospective observational cohort study. Lancet Microbe 2022; 3:e857–e866 [View Article] [PubMed]
     [Google Scholar]
  42. Zeng L, Yang C, Zhang J, Hu K, Zou J et al. An outbreak of carbapenem-resistant Klebsiella pneumoniae in an intensive care unit of a major teaching hospital in Chongqing, China. Front Cell Infect Microbiol 2021; 11:656070 [View Article] [PubMed]
     [Google Scholar]
  43. Paul M, Daikos GL, Durante-Mangoni E, Yahav D, Carmeli Y et al. Colistin alone versus colistin plus meropenem for treatment of severe infections caused by carbapenem-resistant Gram-negative bacteria: an open-label, randomised controlled trial. Lancet Infect Dis 2018; 18:391–400 [View Article] [PubMed]
     [Google Scholar]
  44. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B et al. The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio 2013; 4:e00377-13 [View Article] [PubMed]
     [Google Scholar]
  45. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE et al. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. mBio 2016; 7:e02162 [View Article] [PubMed]
     [Google Scholar]
  46. Muller A, Gbaguidi-Haore H, Cholley P, Hocquet D, Sauget M et al. Hospital-diagnosed infections with Escherichia coli clonal group ST131 are mostly acquired in the community. Sci Rep 2021; 11:5702 [View Article] [PubMed]
     [Google Scholar]
  47. Oteo J, Alcaraz R, Bou G, Conejo C, Díaz-Lamas AM et al. Rates of faecal colonization by carbapenemase-producing Enterobacteriaceae among patients admitted to ICUs in Spain. J Antimicrob Chemother 2015; 70:2916–2918 [View Article] [PubMed]
     [Google Scholar]
  48. Wyres KL, Hawkey J, Mirčeta M, Judd LM, Wick RR et al. Genomic surveillance of antimicrobial resistant bacterial colonisation and infection in intensive care patients. BMC Infect Dis 2021; 21:683 [View Article] [PubMed]
     [Google Scholar]
  49. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M et al. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci U S A 2014; 111:5694–5699 [View Article] [PubMed]
     [Google Scholar]
  50. Qin X, Wu S, Hao M, Zhu J, Ding B et al. The colonization of carbapenem-resistant Klebsiella pneumoniae: epidemiology, resistance mechanisms, and risk factors in patients admitted to intensive care units in China. J Infect Dis 2020; 221:S206–S214 [View Article] [PubMed]
     [Google Scholar]
  51. Boonyasiri A, Jauneikaite E, Brinkac LM, Greco C, Lerdlamyong K et al. Genomic and clinical characterisation of multidrug-resistant carbapenemase-producing ST231 and ST16 Klebsiella pneumoniae isolates colonising patients at Siriraj hospital, Bangkok, Thailand from 2015 to 2017. BMC Infect Dis 2021; 21:142 [View Article] [PubMed]
     [Google Scholar]
  52. Lapp Z, Crawford R, Miles-Jay A, Pirani A, Trick WE et al. Regional spread of blaNDM-1-containing Klebsiella pneumoniae ST147 in post-acute care facilities. Clin Infect Dis 2021; 73:1431–1439 [View Article] [PubMed]
     [Google Scholar]
  53. Gorrie CL, Mirčeta M, Wick RR, Judd LM, Lam MMC et al. Genomic dissection of Klebsiella pneumoniae infections in hospital patients reveals insights into an opportunistic pathogen. Nat Commun 2022; 13:3017 [View Article] [PubMed]
     [Google Scholar]
  54. Mavroidi A, Liakopoulos A, Gounaris A, Goudesidou M, Gaitana K et al. Successful control of a neonatal outbreak caused mainly by ST20 multidrug-resistant SHV-5-producing Klebsiella pneumoniae, Greece. BMC Pediatr 2014; 14:105 [View Article] [PubMed]
     [Google Scholar]
  55. Pei N, Li Y, Liu C, Jian Z, Liang T et al. Large-scale genomic epidemiology of Klebsiella pneumoniae identified clone divergence with hypervirulent plus antimicrobial-resistant characteristics causing within-ward strain transmissions. Microbiol Spectr 2022; 10:e0269821 [View Article] [PubMed]
     [Google Scholar]
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Longitudinal genomic surveillance of a UK intensive care unit shows a lack of patient colonisation by multi-drug-resistant Gram-negative bacterial pathogens
M Gen 10, 001314 (2024); https://doi.org/10.1099/mgen.0.001314
/content/journal/mgen/10.1099/mgen.0.001314
/content/journal/mgen/10.1099/mgen.0.001314
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