Colonisation of hospital surfaces from low- and middle-income countries by extended spectrum β-lactamase- and carbapenemase-producing bacteria.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
29 Mar 2024
Historique:
received: 27 07 2023
accepted: 06 03 2024
medline: 30 3 2024
pubmed: 30 3 2024
entrez: 30 3 2024
Statut: epublish

Résumé

Hospital surfaces can harbour bacterial pathogens, which may disseminate and cause nosocomial infections, contributing towards mortality in low- and middle-income countries (LMICs). During the BARNARDS study, hospital surfaces from neonatal wards were sampled to assess the degree of environmental surface and patient care equipment colonisation by Gram-negative bacteria (GNB) carrying antibiotic resistance genes (ARGs). Here, we perform PCR screening for extended-spectrum β-lactamases (bla

Identifiants

pubmed: 38553439
doi: 10.1038/s41467-024-46684-z
pii: 10.1038/s41467-024-46684-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2758

Subventions

Organisme : Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)
ID : OPP1119772
Organisme : Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)
ID : OP1191522

Informations de copyright

© 2024. The Author(s).

Références

Acolatse, J. E. E. et al. Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital. Antimicrob. Resist. Infect. Control 11, 49 (2022).
Dancer, S. J. The role of environmental cleaning in the control of hospital-acquired infection. J. Hosp. Infect. 73, 378–385 (2009).
pubmed: 19726106 doi: 10.1016/j.jhin.2009.03.030
Zahornacký, O., Porubčin, Š., Rovňáková, A. & Jarčuška, P. Gram-Negative rods on inanimate surfaces of selected hospital facilities and their nosocomial significance. Int. J. Environ. Res. Public. Health 19, 6039 (2022).
pubmed: 35627578 pmcid: 9141962 doi: 10.3390/ijerph19106039
CDC and ICAN. Best Practices for Environmental Cleaning in Resource-Limited Healthcare Settings. A Healthcare Cleaning and Disinfection Guide for Healthcare Settings with Limited Resources (CDC and ICAN, 2023).
Boyce, J. M. Alcohols as surface disinfectants in healthcare settings. Infect. Control Hosp. Epidemiol. 39, 323–328 (2018).
pubmed: 29374503 doi: 10.1017/ice.2017.301
World Health Organization. Standard Precautions for the Prevention and Control of Infections: Aide-Memoire (World Health Organization, 2022).
Carvalho, M. J. et al. Antibiotic resistance genes in the gut microbiota of mothers and linked neonates with or without sepsis from low- and middle-income countries. Nat. Microbiol. 7, 1337–1347 (2022).
pubmed: 35927336 pmcid: 9417982 doi: 10.1038/s41564-022-01184-y
Mukherjee, S., Mitra, S., Dutta, S. & Basu, S. Neonatal sepsis: the impact of carbapenem-resistant and hypervirulent Klebsiella pneumoniae. Front. Med. 8, 634349 (2021).
doi: 10.3389/fmed.2021.634349
Musoke, D. et al. The role of Environmental Health in preventing antimicrobial resistance in low- and middle-income countries. Environ. Health Prev. Med. 26, 100 (2021).
Rudd, K. E. et al. Global, regional, and national sepsis incidence and mortality, 1990–2017: analysis for the Global Burden of Disease Study. Lancet 395, 200–211 (2020).
pubmed: 31954465 pmcid: 6970225 doi: 10.1016/S0140-6736(19)32989-7
Sands, K. et al. Early-onset neonatal sepsis in low- and middle-income countries: current challenges and future opportunities. Infect. Drug Resist. 15, 933–946 (2022).
pubmed: 35299860 pmcid: 8921667 doi: 10.2147/IDR.S294156
Shao, Y. et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature 574, 117–121 (2019).
pubmed: 31534227 pmcid: 6894937 doi: 10.1038/s41586-019-1560-1
World Health Organization. Minimum Requirements for Infection Prevention and Control Programmes (World Health Organization, Geneva, 2019).
World Health Organization. Pocket Book of Hospital Care for Children. Guidelines for the Management of Common Childhood Illnesses (World Health Organization, Geneva, 2013).
Farzana, R. et al. Outbreak of hypervirulent multidrug-resistant Klebsiella variicola causing high mortality in neonates in Bangladesh. Clin. Infect. Dis. 68, 1225–1227 (2019).
pubmed: 30204843 doi: 10.1093/cid/ciy778
Firesbhat, A., Tigabu, A., Tegene, B. & Gelaw, B. Bacterial profile of high-touch surfaces, leftover drugs and antiseptics together with their antimicrobial susceptibility patterns at University of Gondar Comprehensive Specialized Hospital, Northwest Ethiopia. BMC Microbiol. 21, 309 (2021).
pubmed: 34749674 pmcid: 8573887 doi: 10.1186/s12866-021-02378-w
Silago, V. et al. Predominance of Acinetobacter spp., Harboring the blaIMP gene, contaminating the hospital environment in a tertiary hospital in Mwanza, Tanzania: a cross-sectional laboratory-based study. Pathogens 11, 63 (2022).
pubmed: 35056011 pmcid: 8781992 doi: 10.3390/pathogens11010063
World Health Organization. Guidelines for the Prevention and Control of Carbapenem-Resistant Enterobacteriaceae, Acinetobacter Baumannii and Pseudomonas Aeruginosa in Health Care Facilities (World Health Organization, Geneva, 2017).
World Health Organization. Report on the Burden of Endemic Health Care-Associated Infection Worldwide (World Health Organization, Geneva, 2011).
Chaoui, L., Mhand, R., Mellouki, F. & Rhallabi, N. Contamination of the surfaces of a health care environment by Multidrug-Resistant (MDR) bacteria. Int. J. Microbiol. 2019, 1–7 (2019).
doi: 10.1155/2019/3236526
Won, S. Y. et al. Emergence and rapid regional spread of Klebsiella pneumoniae carbapenemase-producing enterobacteriaceae. Clin. Infect. Dis. 53, 532–540 (2011).
pubmed: 21865189 doi: 10.1093/cid/cir482
World Health Organization. Global Report on the Epidemiology and Burden of Sepsis. https://www.who.int/publications-detail-redirect/9789240010789 (World Health Organization, 2020).
Farzana, R., Swedberg, G., Giske, C. G. & Hasan, B. Molecular and genetic characterization of emerging carbapenemase-producing Acinetobacter baumannii strains from patients and hospital environments in Bangladesh. Infect. Prev. Pract. 4, 100215 (2022).
pubmed: 35603008 pmcid: 9118665 doi: 10.1016/j.infpip.2022.100215
Darge, A., Kahsay, A. G., Hailekiros, H., Niguse, S. & Abdulkader, M. Bacterial contamination and antimicrobial susceptibility patterns of intensive care units medical equipment and inanimate surfaces at Ayder Comprehensive Specialized Hospital, Mekelle, Northern Ethiopia. BMC Res. Notes 12, 621 (2019).
pubmed: 31547851 pmcid: 6757422 doi: 10.1186/s13104-019-4658-5
Zubair, M. et al. Role of hospital surfaces in transmission of infectious diseases. Pak. J. Med. Health Sci. 12, 857–859 (2018).
Sands, K. et al. Characterization of antimicrobial-resistant Gram-negative bacteria that cause neonatal sepsis in seven low- and middle-income countries. Nat. Microbiol. 6, 512–523 (2021).
pubmed: 33782558 pmcid: 8007471 doi: 10.1038/s41564-021-00870-7
Farzana, R. et al. Emergence of mobile colistin resistance (mcr-8) in a highly successful Klebsiella pneumoniae sequence type 15 clone from clinical infections in Bangladesh. mSphere 5, e00023–20 (2020).
pubmed: 32161143 pmcid: 7067589 doi: 10.1128/mSphere.00023-20
Lam, M. M. C. et al. A genomic surveillance framework and genotyping tool for Klebsiella pneumoniae and its related species complex. Nat. Commun. 12, 4188 (2021).
pubmed: 34234121 pmcid: 8263825 doi: 10.1038/s41467-021-24448-3
Wyres, K. L., Lam, M. M. C. & Holt, K. E. Population genomics of Klebsiella pneumoniae. Nat. Rev. Microbiol. 18, 344–359 (2020).
pubmed: 32055025 doi: 10.1038/s41579-019-0315-1
Lam, M. M. C. et al. Tracking key virulence loci encoding aerobactin and salmochelin siderophore synthesis in Klebsiella pneumoniae. Genome Med. 10, 77 (2018).
pubmed: 30371343 pmcid: 6205773 doi: 10.1186/s13073-018-0587-5
Ekwanzala, M. D., Dewar, J. B., Kamika, I. & Momba, M. N. B. Tracking the environmental dissemination of carbapenem-resistant Klebsiella pneumoniae using whole genome sequencing. Sci. Total Environ. 691, 80–92 (2019).
pubmed: 31319261 doi: 10.1016/j.scitotenv.2019.06.533
Obasi, A. et al. Extended-spectrum β-lactamase-producing Klebsiella pneumoniae from pharmaceutical wastewaters in South-Western Nigeria. Microb. Drug Resist. 23, 1013–1018 (2017).
pubmed: 28375698 doi: 10.1089/mdr.2016.0269
World Health Organization. Guidelines on Core Components of Infection Prevention and Control Programmes at the National and Acute Health Care Facility Level (World Health Organization, Geneva, 2016).
World Health Organization. Global Report on Infection Prevention and Control (World Health Organization, 2022).
Costa, D. M. et al. Biofilm contamination of high‐touched surfaces in intensive care units: epidemiology and potential impacts. Lett. Appl. Microbiol. 68, 269–276 (2019).
pubmed: 30758060 doi: 10.1111/lam.13127
Yusha’u, M., Bukar, A., Aliyu, B. S. & Abdulkareem, A. Bacterial contamination of some hospital equipments in Kano, Nigeria. Hamdard Med. 55, 39–42 (2012).
Munyeshyaka, E., Cyuzuzo, P., Yadufashije, C. & Karemera, J. Contribution of medical wards contamination to wound infection among patients attending Ruhengeri Referral Hospital. Int. J. Microbiol. 2021, 7 (2021).
doi: 10.1155/2021/7838763
Owusu, E., Asane, F. W., Bediako-Bowan, A. A. & Afutu, E. Bacterial contamination of surgical instruments used at the surgery Department of a Major Teaching Hospital in a Resource-Limited Country: an observational study. Diseases 10, 81 (2022).
pubmed: 36278580 pmcid: 9589928 doi: 10.3390/diseases10040081
Shiferaw, T., Beyene, G., Kassa, T. & Sewunet, T. Bacterial contamination, bacterial profile and antimicrobial susceptibility pattern of isolates from stethoscopes at Jimma University Specialized Hospital. Ann. Clin. Microbiol. Antimicrob. 12, 39 (2013).
pubmed: 24330702 pmcid: 3880102 doi: 10.1186/1476-0711-12-39
Thomson, K. M. et al. Effects of antibiotic resistance, drug target attainment, bacterial pathogenicity and virulence, and antibiotic access and affordability on outcomes in neonatal sepsis: an International Microbiology and Drug Evaluation Prospective substudy (BARNARDS). Lancet Infect. Dis. 21, 1677–1688 (2021).
pubmed: 34384533 pmcid: 8612937 doi: 10.1016/S1473-3099(21)00050-5
Aleem, M. et al. Prevalence of bacteria and antimicrobial resistance genes in hospital water and surfaces. Cureus 13, 10 (2021).
Mahmud, Z. H. et al. Healthcare facilities as potential reservoirs of antimicrobial resistant Klebsiella pneumoniae: an emerging concern to public health in Bangladesh. Pharmaceuticals 15, 1116 (2022).
pubmed: 36145337 pmcid: 9504507 doi: 10.3390/ph15091116
Boostrom, I., Portal, E. A. R., Spiller, O. B., Walsh, T. R. & Sands, K. Comparing long-read assemblers to explore the potential of a sustainable low-cost, low-infrastructure approach to sequence antimicrobial resistant bacteria with Oxford nanopore sequencing. Front. Microbiol. 13, 796465 (2022).
pubmed: 35308384 pmcid: 8928191 doi: 10.3389/fmicb.2022.796465
Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).
pubmed: 23422339 pmcid: 3624806 doi: 10.1093/bioinformatics/btt086
Pathogenwatch. A global platform for genomic Surveillance https://pathogen.watch/ (2023).
Seemann T. ABRicate. Mass Screening of Contigs for Antimicrobial and Virulence Genes https://github.com/tseemann/abricate (2016).
Feldgarden, M. et al. Validating the AMRFinder tool and resistance gene database by using antimicrobial resistance genotype–phenotype correlations in a collection of isolates. Antimicrob. Agents Chemother. 63, e00483–19 (2019).
pubmed: 31427293 pmcid: 6811410 doi: 10.1128/AAC.00483-19
Carattoli, A. et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903 (2014).
pubmed: 24777092 pmcid: 4068535 doi: 10.1128/AAC.02412-14
Alcock, B. P. et al. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the Comprehensive Antibiotic Resistance Database. Nucleic Acids Res. 51, 690–699 (2023).
doi: 10.1093/nar/gkac920
Maiden, M. C. J. et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat. Rev. Microbiol. 11, 728–736 (2013).
pubmed: 23979428 pmcid: 3980634 doi: 10.1038/nrmicro3093
Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
pubmed: 24642063 doi: 10.1093/bioinformatics/btu153
Snippy, S. T. Rapid Haploid Variant Calling and Core Genome Alignment https://github.com/tseemann/snippy (2015).
Bush, S. J. et al. Genomic diversity affects the accuracy of bacterial single-nucleotide polymorphism–calling pipelines. GigaScience 9, 1–21 (2020).
doi: 10.1093/gigascience/giaa007
GitHub—tseemann/snp-dists. Pairwise SNP distance matrix from a FASTA sequence alignment. https://github.com/tseemann/snp-dists (2021).
Darling, A. C. E., Mau, B., Blattner, F. R. & Perna, N. T. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394–1403 (2004).
pubmed: 15231754 pmcid: 442156 doi: 10.1101/gr.2289704
Ondov, B. D. et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 17, 132 (2016).
pubmed: 27323842 pmcid: 4915045 doi: 10.1186/s13059-016-0997-x
Chemaly, R. F. et al. The role of the healthcare environment in the spread of multidrug-resistant organisms: update on current best practices for containment. Ther. Adv. Infect. Dis. 2, 79–90 (2014).
pubmed: 25469234 pmcid: 4250270
Russotto, V. et al. What healthcare workers should know about environmental bacterial contamination in the Intensive Care Unit. BioMed. Res. Int. 2017, 6905450 (2017).
pubmed: 29214175 pmcid: 5682046 doi: 10.1155/2017/6905450
World Health Organization & WHO Patient Safety. Hand Hygiene Technical Reference Manual: to be Used by Health-care Workers, Trainers and Observers of Hand Hygiene Practices (World Health Organization & WHO Patient Safety, 2009).
Centers for Disease Control and Prevention (CDC). Public Health Strategies to Prevent the Spread of Novel and Targeted Multidrug-resistant Organisms (MDROs) (Centers for Disease Control and Prevention (CDC), 2023).
Centers for Disease Control and Prevention (CDC). Preventing Healthcare-Associated Infections. Reduce Risk from Water (Centers for Disease Control and Prevention (CDC), 2023).
World Bank Climate Change Knowledge Portal. https://climateknowledgeportal.worldbank.org/ (2021).

Auteurs

Maria Nieto-Rosado (M)

Department of Biology, Ineos Oxford Institute for Antimicrobial Research, University of Oxford, Oxford, UK. maria.nietorosado@biology.ox.ac.uk.
Division of Infection and Immunity, Cardiff University, Cardiff, UK. maria.nietorosado@biology.ox.ac.uk.

Kirsty Sands (K)

Department of Biology, Ineos Oxford Institute for Antimicrobial Research, University of Oxford, Oxford, UK.
Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Edward A R Portal (EAR)

Department of Biology, Ineos Oxford Institute for Antimicrobial Research, University of Oxford, Oxford, UK.
Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Kathryn M Thomson (KM)

Department of Biology, Ineos Oxford Institute for Antimicrobial Research, University of Oxford, Oxford, UK.
Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Maria J Carvalho (MJ)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.
Department of Medical Sciences, Institute of Biomedicine, University of Aveiro, Aveiro, Portugal.

Jordan Mathias (J)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Rebecca Milton (R)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.
Centre for Trials Research, Cardiff University, Cardiff, UK.

Calie Dyer (C)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.
Centre for Trials Research, Cardiff University, Cardiff, UK.

Chinenye Akpulu (C)

Department of Biology, Ineos Oxford Institute for Antimicrobial Research, University of Oxford, Oxford, UK.
Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Ian Boostrom (I)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Patrick Hogan (P)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Habiba Saif (H)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Ana D Sanches Ferreira (AD)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.
Parasites and Microbes Programme, Wellcome Sanger Institute Hinxton, Hinxton, UK.

Thomas Hender (T)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Barbra Portal (B)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Robert Andrews (R)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

W John Watkins (WJ)

Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Rabaab Zahra (R)

Department of Microbiology, Quaid-i-Azam University, Islamabad, Pakistan.

Haider Shirazi (H)

Pakistan Institute of Medical Sciences, Islamabad, Pakistan.

Adil Muhammad (A)

Department of Microbiology, Quaid-i-Azam University, Islamabad, Pakistan.

Syed Najeeb Ullah (SN)

Department of Microbiology, Quaid-i-Azam University, Islamabad, Pakistan.

Muhammad Hilal Jan (MH)

Department of Microbiology, Quaid-i-Azam University, Islamabad, Pakistan.

Shermeen Akif (S)

Department of Microbiology, Quaid-i-Azam University, Islamabad, Pakistan.

Kenneth C Iregbu (KC)

National Hospital Abuja, Abuja, Nigeria.

Fatima Modibbo (F)

Débbo Africa, Lekki, Lagos, Nigeria.

Stella Uwaezuoke (S)

Federal Medical Centre Jabi, Abuja, Nigeria.

Lamidi Audu (L)

National Hospital Abuja, Abuja, Nigeria.

Chinago P Edwin (CP)

Department of Microbiology, Medway Maritime Hospital NHS Foundation Trust, Gillingham, Kent, UK.
Aminu Kano Teaching Hospital, Kano, Nigeria.

Ashiru H Yusuf (AH)

Aminu Kano Teaching Hospital, Kano, Nigeria.

Adeola Adeleye (A)

Murtala Muhammad Specialist Hospital, Kano City, Nigeria.

Aisha S Mukkadas (AS)

Murtala Muhammad Specialist Hospital, Kano City, Nigeria.

Jean Baptiste Mazarati (JB)

The National Reference Laboratory, Rwanda Biomedical Centre, Kigali, Rwanda.

Aniceth Rucogoza (A)

The National Reference Laboratory, Rwanda Biomedical Centre, Kigali, Rwanda.

Lucie Gaju (L)

The National Reference Laboratory, Rwanda Biomedical Centre, Kigali, Rwanda.

Shaheen Mehtar (S)

Unit of IPC, Stellenbosch University, Cape Town, South Africa.
Infection Control Africa Network, Cape Town, South Africa.

Andrew N H Bulabula (ANH)

Infection Control Africa Network, Cape Town, South Africa.
Department of Global Health, Stellenbosch University, Cape Town, South Africa.

Andrew Whitelaw (A)

Division of Medical Microbiology, Stellenbosch University, Cape Town, South Africa.
National Health Laboratory Service, Tygerberg Hospital, Cape Town, South Africa.

Lauren Roberts (L)

Division of Medical Microbiology, Stellenbosch University, Cape Town, South Africa.

Grace Chan (G)

Department of Pediatrics, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA.
Department of Pediatrics and Child Health, St Paul's Hospital Millennium Medical College, Addis Ababa, Ethiopia.

Delayehu Bekele (D)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, USA.
Department of Obstetrics and Gynecology, St Paul's Hospital Millennium Medical College, Addis Ababa, Ethiopia.

Semaria Solomon (S)

Department of Microbiology, Immunology and Parasitology, St Paul's Hospital Millennium Medical College, Addis Ababa, Ethiopia.

Mahlet Abayneh (M)

Department of Pediatrics and Child Health, St Paul's Hospital Millennium Medical College, Addis Ababa, Ethiopia.

Gesit Metaferia (G)

Department of Microbiology, Immunology and Parasitology, St Paul's Hospital Millennium Medical College, Addis Ababa, Ethiopia.

Timothy R Walsh (TR)

Department of Biology, Ineos Oxford Institute for Antimicrobial Research, University of Oxford, Oxford, UK.
Division of Infection and Immunity, Cardiff University, Cardiff, UK.

Classifications MeSH