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Abstract

In 2022, an outbreak with severe bloodstream infections caused by occurred in an adult intensive care unit (ICU) in Hungary. Eight cases, five of whom died, were detected. Initial control measures could not stop the outbreak. We conducted a matched case–control study. In univariable analysis, the cases were more likely to be located around one sink in the ICU and had more medical procedures and medications than the controls, however, the multivariable analysis was not conclusive. Isolates from blood cultures of the cases and the ICU environment were closely related by whole genome sequencing and resistant or tolerant against the quaternary ammonium compound surface disinfectant used in the ICU. Thus, was able to survive in the environment despite regular cleaning and disinfection. The hospital replaced the disinfectant with another one, tightened the cleaning protocol and strengthened hand hygiene compliance among the healthcare workers. Together, these control measures have proved effective to prevent new cases. Our results highlight the importance of multidisciplinary outbreak investigations, including environmental sampling, molecular typing and testing for disinfectant resistance.

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/content/10.2807/1560-7917.ES.2024.29.26.2300492
2024-06-27
2024-07-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.26.2300492
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References

  1. Vonberg RP, Weitzel-Kage D, Behnke M, Gastmeier P. Worldwide Outbreak Database: the largest collection of nosocomial outbreaks. Infection. 2011;39(1):29-34.  https://doi.org/10.1007/s15010-010-0064-6  PMID: 21153042 
  2. European Centre for Disease Prevention Control (ECDC). Healthcare-associated infections acquired in intensive care units. ECDC Annual Epidemiological Report for 2018. Stockholm: ECDC; 5 May 2023. Available from: https://www.ecdc.europa.eu/en/publications-data/healthcare-associated-infections-intensive-care-units-annual-report-2018#:~:text=In%3A%20ECDC.-,Annual%20epidemiological%20report%20for,Stockholm%3A%20ECDC%3B%202023.&text=In%202018%2C%209%20860%20(7.8,infection%20or%20urinary%20tract%20infection)
  3. Nemzeti Jogszabálytár. 20/2009, VI. 18, EüM rendelet az egészségügyi ellátással összefüggő fertőzések megelőzéséről, e tevékenységek szakmai minimumfeltételeiről és felügyeletéről. [20/2009, VI. 18., EüM regulation on the prevention of healthcare-associated infections, and professional minimum requirements and supervision of these activities]. Budapest: Nemzeti Jogszabálytár; 2009. Hungarian. Available from: https://njt.hu/jogszabaly/2009-20-20-0B
  4. National Center for Public Health and Pharmacy (NNGYK). Annual reports of the National Nosocomial Surveillance System. 2016-2021. Budapest: NNGYK; 2022. Hungarian. Available from: https://www.antsz.hu/felso_menu/temaink/jarvany/korhazifert
  5. Macdonald TM, Langley JM, Mailman T, Allain K, Nelson G, Hatton L, et al. Serratia marcescens outbreak in a neonatal intensive care unit related to the exit port of an oscillator. Pediatr Crit Care Med. 2011;12(6):e282-6.  https://doi.org/10.1097/PCC.0b013e31820ac42a  PMID: 21283042 
  6. Choquet M, Mullié C. Down the drain: a systematic review of molecular biology evidence linking sinks with bacterial healthcare-associated infections in intensive care units. Hygiene (Basel). 2022;2(2):94-108.  https://doi.org/10.3390/hygiene2020008 
  7. Suleyman G, Alangaden G, Bardossy AC. The role of environmental contamination in the transmission of nosocomial pathogens and healthcare-associated infections. Curr Infect Dis Rep. 2018;20(6):12.  https://doi.org/10.1007/s11908-018-0620-2  PMID: 29704133 
  8. Kizny Gordon AE, Mathers AJ, Cheong EYL, Gottlieb T, Kotay S, Walker AS, et al. The hospital water environment as a reservoir for carbapenem-resistant organisms causing hospital-acquired infections-a systematic review of the literature. Clin Infect Dis. 2017;64(10):1435-44.  https://doi.org/10.1093/cid/cix132  PMID: 28200000 
  9. Betteridge T, Merlino J, Natoli J, Cheong EY-L, Gottlieb T, Stokes HW. Plasmids and bacterial strains mediating multidrug-resistant hospital-acquired infections are coresidents of the hospital environment. Microb Drug Resist. 2013;19(2):104-9.  https://doi.org/10.1089/mdr.2012.0104  PMID: 23067199 
  10. Mahlen SD. Serratia infections: from military experiments to current practice. Clin Microbiol Rev. 2011;24(4):755-91.  https://doi.org/10.1128/CMR.00017-11  PMID: 21976608 
  11. Cristina ML, Sartini M, Spagnolo AM. Serratia marcescens infections in neonatal intensive care units (NICUs). Int J Environ Res Public Health. 2019;16(4):610.  https://doi.org/10.3390/ijerph16040610  PMID: 30791509 
  12. Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis. 2006;6(1):130.  https://doi.org/10.1186/1471-2334-6-130  PMID: 16914034 
  13. Polilli E, Parruti G, Fazii P, D’Antonio D, Palmieri D, D’Incecco C, et al. Rapidly controlled outbreak of Serratia marcescens infection/colonisations in a neonatal intensive care unit, Pescara General Hospital, Pescara, Italy, April 2011. Euro Surveill. 2011;16(24):19892.  https://doi.org/10.2807/ese.16.24.19892-en  PMID: 21699768 
  14. Szewzyk U, Szewzyk R, Stenström TA. Growth and survival of Serratia marcescens under aerobic and anaerobic conditions in the presence of materials from blood bags. J Clin Microbiol. 1993;31(7):1826-30.  https://doi.org/10.1128/jcm.31.7.1826-1830.1993  PMID: 8349760 
  15. Boyce JM. Quaternary ammonium disinfectants and antiseptics: tolerance, resistance and potential impact on antibiotic resistance. Antimicrob Resist Infect Control. 2023;12(1):32.  https://doi.org/10.1186/s13756-023-01241-z  PMID: 37055844 
  16. Porta MS (ed). A Dictionary of Epidemiology. Oxford: Oxford University Press; 2014.
  17. R Core Team. R: A Language and Environment for Statistical Computing: R Foundation for Statistical Computing, Vienna, Austria; 2022. Available from: https://www.R-project.org/
  18. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 12.0. 2022. Available from: https://www.eucast.org/clinical_breakpoints
  19. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Preparation of agar plates and broth for EUCAST AST. Version 7.0. 1 Jan 2022. Available from: https://www.eucast.org/ast_of_bacteria/media_preparation
  20. European Chemicals Agency (ECHA). Substance Infocard for Quaternary ammonium compounds, benzyl-C12-16-alkyldimethyl, chlorides. Helsinki: ECHA; 30 Jan 2024. Available from: https://echa.europa.eu/substance-information/-/substanceinfo/100.063.913
  21. European Chemicals Agency (ECHA). Substance Infocard for polyhexamethylene biguanide hydrochloride PHMB. Helsinki: ECHA; 27 Jun 2023. Available from: https://echa.europa.eu/substance-information/-/substanceinfo/100.115.789
  22. Centers for Disease Control and Prevention (CDC). PulseNet Quality Assurance/Quality Control (QA/QC) Manual, version 2.0 for the Centers for Disease Control and Prevention. Atlanta: CDC; 9 May 2005. Available from: https://pulsenetinternational.org/assets/PulseNet/uploads/QAQC/PulseNet-QAQC-Manual.pdf
  23. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008;9(1):75.  https://doi.org/10.1186/1471-2164-9-75  PMID: 18261238 
  24. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Expert Rules v 3.2 on Enterobacterales. Jan 2023. Available from: https://www.eucast.org/expert_rules_and_expected_phenotypes
  25. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268-81.  https://doi.org/10.1111/j.1469-0691.2011.03570.x  PMID: 21793988 
  26. Mardanova AM, Bogomol’naya LM, Romanova YD, Sharipova MR. Efflux systems in Serratia marcescens. Microbiology (N Y). 2013;82(6):668-79.  https://doi.org/10.1134/S0026261714010093 
  27. Itoh Y, Rice JD, Goller C, Pannuri A, Taylor J, Meisner J, et al. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-β-1,6-N-acetyl-D-glucosamine. J Bacteriol. 2008;190(10):3670-80.  https://doi.org/10.1128/JB.01920-07  PMID: 18359807 
  28. Kümmerle N, Feucht HH, Kaulfers PM. Plasmid-mediated formaldehyde resistance in Escherichia coli: characterization of resistance gene. Antimicrob Agents Chemother. 1996;40(10):2276-9.  https://doi.org/10.1128/AAC.40.10.2276  PMID: 8891129 
  29. Hanczvikkel A, Füzi M, Ungvári E, Tóth Á. Transmissible silver resistance readily evolves in high-risk clone isolates of Klebsiella pneumoniae. Acta Microbiol Immunol Hung. 2018;65(3):387-403.  https://doi.org/10.1556/030.65.2018.031  PMID: 30043621 
  30. European Chemicals Agency (ECHA). Substance Infocard for sodium dichloroisocyanurate dehydrate. Helsinki: ECHA; 15 Jan 2024. Available from: https://echa.europa.eu/hu/substance-information/-/substanceinfo/100.106.495
  31. European Chemicals Agency (ECHA). Substance Infocard for Quaternary ammonium compounds, benzyl-C12-18-alkyldimethyl, chlorides. Helsinki: ECHA; 6 Sep 2023. Available from: https://echa.europa.eu/hu/substance-information/-/substanceinfo/100.063.544
  32. European Chemicals Agency (ECHA). Substance Infocard for N-(3-aminopropyl)-N-dodecylpropane-1,3-diamine. Helsinki: ECHA; 6 Sep 2023. Available from: https://echa.europa.eu/hu/substance-information/-/substanceinfo/100.017.406
  33. Iovene MR, Pota V, Galdiero M, Corvino G, Di Lella FM, Stelitano D, et al. First Italian outbreak of VIM-producing Serratia marcescens in an adult polyvalent intensive care unit, August-October 2018: A case report and literature review. World J Clin Cases. 2019;7(21):3535-48.  https://doi.org/10.12998/wjcc.v7.i21.3535  PMID: 31750335 
  34. Bagattini M, Crispino M, Gentile F, Barretta E, Schiavone D, Boccia MC, et al. A nosocomial outbreak of Serratia marcescens producing inducible Amp C-type beta-lactamase enzyme and carrying antimicrobial resistance genes within a class 1 integron. J Hosp Infect. 2004;56(1):29-36.  https://doi.org/10.1016/j.jhin.2003.07.004  PMID: 14706268 
  35. Holmes CL, Anderson MT, Mobley HLT, Bachman MA. Pathogenesis of Gram-negative bacteremia. Clin Microbiol Rev. 2021;34(2):e00234-20.  https://doi.org/10.1128/CMR.00234-20  PMID: 33692149 
  36. Prado G, Mendes ET, Martins RCR, Perdigão-Neto LV, Freire MP, Marchi AP, et al. Phenotypic and genotypic characteristics of a carbapenem-resistant Serratia marcescens cohort and outbreak: describing an opportunistic pathogen. Int J Antimicrob Agents. 2022;59(1):106463.  https://doi.org/10.1016/j.ijantimicag.2021.106463  PMID: 34715332 
  37. Bourdin T, Benoit , Monnier A, Bédard E, Prévost M, Charron D, et al. Serratia marcescens colonization in a neonatal intensive care unit has multiple sources, with sink drains as a major reservoir. Appl Environ Microbiol. 2023;89(5):e0010523.  https://doi.org/10.1128/aem.00105-23  PMID: 37067412 
  38. Wendel AF, Kolbe-Busch S, Ressina S, Schulze-Röbbecke R, Kindgen-Milles D, Lorenz C, et al. Detection and termination of an extended low-frequency hospital outbreak of GIM-1-producing Pseudomonas aeruginosa ST111 in Germany. Am J Infect Control. 2015;43(6):635-9.  https://doi.org/10.1016/j.ajic.2015.02.024  PMID: 25868648 
  39. Döring G, Ulrich M, Müller W, Bitzer J, Schmidt-Koenig L, Münst L, et al. Generation of Pseudomonas aeruginosa aerosols during handwashing from contaminated sink drains, transmission to hands of hospital personnel, and its prevention by use of a new heating device. Zentralbl Hyg Umweltmed. 1991;191(5-6):494-505. PMID: 1909134 
  40. Kotay SM, Donlan RM, Ganim C, Barry K, Christensen BE, Mathers AJ. Droplet- rather than aerosol-mediated dispersion is the primary mechanism of bacterial transmission from contaminated hand-washing sink traps. Appl Environ Microbiol. 2019;85(2):e01997-18.  https://doi.org/10.1128/AEM.01997-18  PMID: 30367005 
  41. Volling C, Ahangari N, Bartoszko JJ, Coleman BL, Garcia-Jeldes F, Jamal AJ, et al. Are sink drainage systems a reservoir for hospital-acquired gammaproteobacteria colonization and infection? A systematic review. Open Forum Infect Dis. 2020;8(2):ofaa590.  https://doi.org/10.1093/ofid/ofaa590  PMID: 33553469 
  42. Hegstad K, Langsrud S, Lunestad BT, Scheie AA, Sunde M, Yazdankhah SP. Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb Drug Resist. 2010;16(2):91-104.  https://doi.org/10.1089/mdr.2009.0120  PMID: 20370507 
  43. van Dijk HFG, Verbrugh HA, Ad hoc advisory committee on disinfectants of the Health Council of the Netherlands. Resisting disinfectants. Commun Med (Lond). 2022;2(1):6.  https://doi.org/10.1038/s43856-021-00070-8  PMID: 35603291 
  44. Boyce JM, Havill NL. In-use contamination of a hospital-grade disinfectant. Am J Infect Control. 2022;50(12):1296-301.  https://doi.org/10.1016/j.ajic.2022.03.008  PMID: 35307473 
  45. Haller S, Eller C, Hermes J, Kaase M, Steglich M, Radonić A, et al. What caused the outbreak of ESBL-producing Klebsiella pneumoniae in a neonatal intensive care unit, Germany 2009 to 2012? Reconstructing transmission with epidemiological analysis and whole-genome sequencing. BMJ Open. 2015;5(5):e007397.  https://doi.org/10.1136/bmjopen-2014-007397  PMID: 25967999 
  46. Blot S, Ruppé E, Harbarth S, Asehnoune K, Poulakou G, Luyt CE, 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.  https://doi.org/10.1016/j.iccn.2022.103227  PMID: 35249794 
  47. European Centre for Disease Prevention and Control (ECDC). Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals, 2016-2017. Stockholm: ECDC; 5 May 2023. Available from: https://www.ecdc.europa.eu/en/publications-data/point-prevalence-survey-healthcare-associated-infections-and-antimicrobial-use-5
  48. Timsit J-F, Ruppé E, Barbier F, Tabah A, Bassetti M. Bloodstream infections in critically ill patients: an expert statement. Intensive Care Med. 2020;46(2):266-84.  https://doi.org/10.1007/s00134-020-05950-6  PMID: 32047941 
  49. Gahlot R, Nigam C, Kumar V, Yadav G, Anupurba S. Catheter-related bloodstream infections. Int J Crit Illn Inj Sci. 2014;4(2):162-7.  https://doi.org/10.4103/2229-5151.134184  PMID: 25024944 
  50. Faculty of Intensive Care Medicine. Guidelines for the provision of intensive care services. London: Faculty of Intensive Care Medicine; 2022. Available from: https://ficm.ac.uk/standards/guidelines-for-the-provision-of-intensive-care-services
  51. Stahmeyer JT, Lutze B, von Lengerke T, Chaberny IF, Krauth C. Hand hygiene in intensive care units: a matter of time? J Hosp Infect. 2017;95(4):338-43.  https://doi.org/10.1016/j.jhin.2017.01.011  PMID: 28246001 
  52. Chang NN, Schweizer ML, Reisinger HS, Jones M, Chrischilles E, Chorazy M, et al. The impact of workload on hand hygiene compliance: Is 100% compliance achievable? Infect Control Hosp Epidemiol. 2022;43(9):1259-61.  https://doi.org/10.1017/ice.2021.179  PMID: 33985603 
  53. Nemzeti Jogszabálytár. N. 18/1998. (VI. 3.) NM rendelet a fertőző betegségek és a járványok megelőzése érdekében szükséges járványügyi intézkedésekről [18/1998 (VI. 3.). [Regulation on epidemiological measures necessary for the prevention of communicable diseases and outbreaks]: Budapest: Nemzeti Jogszabálytár; 1998. Hungarian. Available from: https://njt.hu/jogszabaly/1998-18-20-3D
  54. National Center for Public Health and Pharmacy (NNGYK). Nemzeti Nosocomialis Surveillance Rendszer, Nosocomialis járványok surveillance modul. Jelentési útmutató, v1.0. [National Nosocomial Surveillance System, Nosocomial outbreak surveillance module. Reporting guideline, v1.0]. Budapest: NNGYK; 2020. Hungarian.
  55. Mermel LA. What is the predominant source of intravascular catheter infections? Clin Infect Dis. 2011;52(2):211-2.  https://doi.org/10.1093/cid/ciq108  PMID: 21288845 
  56. Harnett SJ, Allen KD, Macmillan RR. Critical care unit outbreak of Serratia liquefaciens from contaminated pressure monitoring equipment. J Hosp Infect. 2001;47(4):301-7.  https://doi.org/10.1053/jhin.2001.0941  PMID: 11289774 
  57. Staats GJ. Evaluating the role of efflux pumps in bacterial disinfectant resistance. Bloemfontein University of the Free State; 2022. Available from: https://scholar.ufs.ac.za/items/aebe14f8-ed70-4ad1-a88f-62e112db3e03
  58. Auda IG, Salman IMA, Odah JG. Efflux pumps of Gram-negative bacteria in brief. Gene Rep. 2020;20:100666.  https://doi.org/10.1016/j.genrep.2020.100666 
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