Sanitary installations and wastewater plumbing as reservoir for the long-term circulation and transmission of carbapenemase producing Citrobacter freundii clones in a hospital setting.
CPE
Carbapenemase-producing Enterobacterales
CgMLST
Citrobacter freundii
Hospital
OXA-48
Outbreak
Toilet
WGS
Wastewater collection system
Journal
Antimicrobial resistance and infection control
ISSN: 2047-2994
Titre abrégé: Antimicrob Resist Infect Control
Pays: England
ID NLM: 101585411
Informations de publication
Date de publication:
19 06 2023
19 06 2023
Historique:
received:
20
01
2023
accepted:
29
05
2023
medline:
21
6
2023
pubmed:
20
6
2023
entrez:
19
6
2023
Statut:
epublish
Résumé
Accumulating evidence shows a role of the hospital wastewater system in the spread of multidrug-resistant organisms, such as carbapenemase producing Enterobacterales (CPE). Several sequential outbreaks of CPE on the geriatric ward of the Ghent University hospital have led to an outbreak investigation. Focusing on OXA-48 producing Citrobacter freundii, the most prevalent species, we aimed to track clonal relatedness using whole genome sequencing (WGS). By exploring transmission routes we wanted to improve understanding and (re)introduce targeted preventive measures. Environmental screening (toilet water, sink and shower drains) was performed between 2017 and 2021. A retrospective selection was made of 53 Citrobacter freundii screening isolates (30 patients and 23 environmental samples). DNA from frozen bacterial isolates was extracted and prepped for shotgun WGS. Core genome multilocus sequence typing was performed with an in-house developed scheme using 3,004 loci. The CPE positivity rate of environmental screening samples was 19.0% (73/385). Highest percentages were found in the shower drain samples (38.2%) and the toilet water samples (25.0%). Sink drain samples showed least CPE positivity (3.3%). The WGS data revealed long-term co-existence of three patient sample derived C. freundii clusters. The biggest cluster (ST22) connects 12 patients and 8 environmental isolates taken between 2018 and 2021 spread across the ward. In an overlapping period, another cluster (ST170) links eight patients and four toilet water isolates connected to the same room. The third C. freundii cluster (ST421) connects two patients hospitalised in the same room but over a period of one and a half year. Additional sampling in 2022 revealed clonal isolates linked to the two largest clusters (ST22, ST170) in the wastewater collection pipes connecting the rooms. Our findings suggest long-term circulation and transmission of carbapenemase producing C. freundii clones in hospital sanitary installations despite surveillance, daily cleaning and intermittent disinfection protocols. We propose a role for the wastewater drainage system in the spread within and between rooms and for the sanitary installations in the indirect transmission via bioaerosol plumes. To tackle this problem, a multidisciplinary approach is necessary including careful design and maintenance of the plumbing system.
Sections du résumé
BACKGROUND
Accumulating evidence shows a role of the hospital wastewater system in the spread of multidrug-resistant organisms, such as carbapenemase producing Enterobacterales (CPE). Several sequential outbreaks of CPE on the geriatric ward of the Ghent University hospital have led to an outbreak investigation. Focusing on OXA-48 producing Citrobacter freundii, the most prevalent species, we aimed to track clonal relatedness using whole genome sequencing (WGS). By exploring transmission routes we wanted to improve understanding and (re)introduce targeted preventive measures.
METHODS
Environmental screening (toilet water, sink and shower drains) was performed between 2017 and 2021. A retrospective selection was made of 53 Citrobacter freundii screening isolates (30 patients and 23 environmental samples). DNA from frozen bacterial isolates was extracted and prepped for shotgun WGS. Core genome multilocus sequence typing was performed with an in-house developed scheme using 3,004 loci.
RESULTS
The CPE positivity rate of environmental screening samples was 19.0% (73/385). Highest percentages were found in the shower drain samples (38.2%) and the toilet water samples (25.0%). Sink drain samples showed least CPE positivity (3.3%). The WGS data revealed long-term co-existence of three patient sample derived C. freundii clusters. The biggest cluster (ST22) connects 12 patients and 8 environmental isolates taken between 2018 and 2021 spread across the ward. In an overlapping period, another cluster (ST170) links eight patients and four toilet water isolates connected to the same room. The third C. freundii cluster (ST421) connects two patients hospitalised in the same room but over a period of one and a half year. Additional sampling in 2022 revealed clonal isolates linked to the two largest clusters (ST22, ST170) in the wastewater collection pipes connecting the rooms.
CONCLUSIONS
Our findings suggest long-term circulation and transmission of carbapenemase producing C. freundii clones in hospital sanitary installations despite surveillance, daily cleaning and intermittent disinfection protocols. We propose a role for the wastewater drainage system in the spread within and between rooms and for the sanitary installations in the indirect transmission via bioaerosol plumes. To tackle this problem, a multidisciplinary approach is necessary including careful design and maintenance of the plumbing system.
Identifiants
pubmed: 37337245
doi: 10.1186/s13756-023-01261-9
pii: 10.1186/s13756-023-01261-9
pmc: PMC10280848
doi:
Substances chimiques
carbapenemase
EC 3.5.2.6
Wastewater
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
58Informations de copyright
© 2023. The Author(s).
Références
BMC Bioinformatics. 2010 Dec 10;11:595
pubmed: 21143983
BMC Med. 2012 Aug 13;10:89
pubmed: 22889082
Nucleic Acids Res. 2016 Jul 8;44(W1):W246-51
pubmed: 27131357
J Hosp Infect. 2012 Jan;80(1):1-5
pubmed: 22137761
Appl Environ Microbiol. 2020 Jan 7;86(2):
pubmed: 31704681
Microb Genom. 2017 Sep 14;3(10):e000132
pubmed: 29177090
Lancet Infect Dis. 2018 Mar;18(3):318-327
pubmed: 29276051
Antimicrob Agents Chemother. 2011 Jun;55(6):2655-61
pubmed: 21422204
J Infect Public Health. 2022 Feb;15(2):241-244
pubmed: 35065356
Antimicrob Agents Chemother. 2015 Jan;59(1):714-6
pubmed: 25348541
PLoS One. 2017 Feb 10;12(2):e0171556
pubmed: 28187135
Antimicrob Agents Chemother. 2009 Aug;53(8):3365-70
pubmed: 19506063
Genome Res. 2018 Sep;28(9):1395-1404
pubmed: 30049790
BMC Genomics. 2022 Mar 26;23(1):235
pubmed: 35346021
J Hosp Infect. 2020 Oct;106(2):232-239
pubmed: 32707194
J Intern Med. 2015 May;277(5):501-12
pubmed: 25556628
Infect Control Hosp Epidemiol. 2017 Mar;38(3):320-326
pubmed: 27923418
Lancet. 2017 Feb 25;389(10071):805-814
pubmed: 28104287
Front Cell Infect Microbiol. 2021 Nov 11;11:744431
pubmed: 34858870
Sci Total Environ. 2019 Mar 20;657:7-15
pubmed: 30530220
Infect Dis Clin North Am. 2021 Sep;35(3):575-607
pubmed: 34362535
Clin Infect Dis. 2017 May 15;64(10):1435-1444
pubmed: 28200000
Curr Protoc Bioinformatics. 2020 Jun;70(1):e102
pubmed: 32559359
Antimicrob Resist Infect Control. 2023 Apr 15;12(1):33
pubmed: 37061726
Diagn Microbiol Infect Dis. 2013 Feb;75(2):115-20
pubmed: 23290507
Curr Opin Infect Dis. 2013 Aug;26(4):345-51
pubmed: 23806897
Infect Control Hosp Epidemiol. 2014 Feb;35(2):204-6
pubmed: 24442089
Clin Microbiol Infect. 2013 Feb;19(2):E72-9
pubmed: 23231088
J Hosp Infect. 2020 Oct;106(2):271-276
pubmed: 32750383
Front Microbiol. 2020 Jan 31;10:2961
pubmed: 32082262
J Appl Microbiol. 2021 Dec;131(6):2705-2714
pubmed: 33899991
Bioinformatics. 2018 Sep 1;34(17):i884-i890
pubmed: 30423086
J Hosp Infect. 2018 Nov;100(3):e115-e122
pubmed: 29738784
Euro Surveill. 2015;20(45):
pubmed: 26675038
J Hosp Infect. 2020 Mar 31;:
pubmed: 32243955
Infect Control Hosp Epidemiol. 2014 Apr;35(4):445-7
pubmed: 24602956
Euro Surveill. 2021 May;26(21):
pubmed: 34047273
J Hosp Infect. 2018 Mar;98(3):275-281
pubmed: 29104124
J Hazard Mater. 2018 Sep 15;358:389-396
pubmed: 30005250
Antimicrob Resist Infect Control. 2018 Jan 26;7:16
pubmed: 29423191
Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296
pubmed: 33885785
Rev Infect Dis. 1980 Sep-Oct;2(5):746-60
pubmed: 6763304
J Antimicrob Chemother. 2022 Mar 31;77(4):1200-1202
pubmed: 35089339
Euro Surveill. 2019 Feb;24(9):
pubmed: 30862330
Int J Hyg Environ Health. 2022 May;242:113968
pubmed: 35390565
J Hazard Mater. 2022 Sep 5;437:129280
pubmed: 35714537
Appl Microbiol Biotechnol. 2020 Mar;104(5):1871-1881
pubmed: 31927762
Clin Microbiol Rev. 2020 Feb 26;33(2):
pubmed: 32102899
Microb Genom. 2018 Mar;4(3):
pubmed: 29543149
J Antimicrob Chemother. 2018 Jan 01;73(1):84-87
pubmed: 29040585
J Hosp Infect. 2022 Mar;121:57-64
pubmed: 34915050
Infect Control Hosp Epidemiol. 2021 Oct;42(10):1275-1278
pubmed: 33551004
Virulence. 2017 May 19;8(4):460-469
pubmed: 27593176
Appl Environ Microbiol. 2017 Mar 31;83(8):
pubmed: 28235877
J Microbiol Immunol Infect. 2018 Aug;51(4):565-572
pubmed: 28711438
Lancet Infect Dis. 2019 Jun;19(6):580-581
pubmed: 31122775
Appl Environ Microbiol. 2020 Nov 24;86(24):
pubmed: 32917755
BMC Med. 2017 Apr 27;15(1):86
pubmed: 28446169
Antibiotics (Basel). 2022 May 03;11(5):
pubmed: 35625258
Antimicrob Resist Infect Control. 2021 Oct 20;10(1):149
pubmed: 34670621
Clin Infect Dis. 2021 Mar 1;72(5):e158-e161
pubmed: 33211115
Am J Infect Control. 2016 May 1;44(5):539-43
pubmed: 26899297
Clin Microbiol Infect. 2018 Apr;24(4):350-354
pubmed: 29309930
Science. 2003 May 30;300(5624):1404-9
pubmed: 12775833
Genome Biol. 2019 Nov 28;20(1):257
pubmed: 31779668
Curr Infect Dis Rep. 2018 Aug 20;20(10):42
pubmed: 30128678