Skip to main content

Advertisement

SpringerLink
Log in

Extended spectrum beta-lactamase-producing Klebsiella pneumoniae outbreak reveals incubators as pathogen reservoir in neonatal care center

  • Original Article
  • Published:
European Journal of Pediatrics Aims and scope Submit manuscript

Abstract

In the context of a 3-month extended-spectrum beta-lactamase-producing Klebsiella pneumonia (ESBL-KP) outbreak in a neonatal care center (NCC), hygiene practices and hospital environment were investigated. ESBL-KP strains isolated from patients and environment were compared by molecular typing. The density of incidence of multi-drug-resistant bacteria (MDRB) was calculated from January 2014 to September 2016. The 3-month ESBL-KP outbreak involved 19 patients. Clinical strains from the 19 patients displayed the same molecular profile between them, and with a strain isolated from an incubator after cleaning. Furthermore, 52.4% of incubator mattresses were positive for diverse pathogens. Hygiene practices were acceptable except for external practitioners and parents. In addition to classical infection control (IC) measures, the replacement of mattresses and the improvement of incubators disinfection stopped the outbreak. The protocol of disinfection was revised and microbiological control was implemented. A significant decrease of MDRB incidence was concomitant (p value = 0.03219) but 3 months later, MDRB incidence increased again.

Conclusion: This investigation highlighted incubators and mattresses as critical materials associated to infectious risk in NCC. NCC and IC teams should implement efficient protocol for incubators disinfection and monitoring.

What is Known:

• Environment in neonatal intensive care units is often suspected as reservoir for Enterobacteriaceae outbreaks but is scarcely investigated.

• Incubators and mattresses offer wet and warm conditions suitable for pathogens multiplication, but microbiological survey is not performed routinely for assessing bacterial contamination.

What is New:

• Incubators and mattresses serve as reservoir for pathogens and relay in outbreak.

• An infection control protocol associating efficient disinfection and microbiology analysis is proposed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ESBL-KP:

Beta-lactamase-producing Klebsiella pneumonia

HAI:

Healthcare-associated infection

IC:

Infection control

KP:

Klebsiella pneumonia

MALDI-TOF MS:

Matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry

MDRB:

Multi-drug-resistant bacteria

MRSA:

Methicillin-resistant Staphylococcus aureus

MSSA:

Methicillin-susceptible Staphylococcus aureus

NCC:

Neonatal care center

NICU:

Neonatal intensive care unit

NKU:

Neonatal kangaroo unit

NRU:

Neonatal resuscitation unit

PFGE:

Pulsed field gel electrophoresis

VRE:

Vancomycin-resistant Enterococcus

References

  1. APR W (2018) The role of the environment in the spread of healthcare associated infections. J Hosp Infect 100(3):363–364

    Article  Google Scholar 

  2. Bradbury SL, Mack D, Crofts T, Ellison RT III (2014) Potential bloodborne pathogen exposure from occult mattress damage. Am J Infect Control 42(4):421–422

    Article  PubMed  Google Scholar 

  3. Brooks B, Firek BA, Miller CS, Sharon I, Thomas BC, Baker R, Morowitz MJ, Banfield JF (2014) Microbes in the neonatal intensive care unit resembl those found in the gut of premature infants. Microbiome 2:1

    Article  PubMed  PubMed Central  Google Scholar 

  4. Buffet-Bataillon S, Rabier V, Bétrémieux P, Beuchée A, Bauer M, Pladys P, le Gall E, Cormier M, Jolivet-Gougeon A (2009) Outbreak of Serratia marcescens in a neonatal intensive care unit: contaminated unmedicated liquid soap and risk factors. J Hosp Infect 72(1):17–22

    Article  PubMed  CAS  Google Scholar 

  5. Butin M, Martins-Simões P, Picaud JC, Kearns A, Claris O, Vandenesch F, Laurent F, Rasigade JP (2015) Adaptation to vancomycin pressure of multiresistant Staphylococcus capitis NRCS-A involved in neonatal sepsis. J Antimicrob Chemother 70(11):3027–3031

    Article  PubMed  CAS  Google Scholar 

  6. Carey AJ, Saiman L, Polin RA (2008) Hospital-acquired infections in the NICU: epidemiology for the new millennium. Clin Perinatol 35(1):223–249

    Article  PubMed  Google Scholar 

  7. Casolari C, Pecorari M, Della Casa E, Cattani S, Venturelli C, Fabio G, Tagliazucchi S, Serpini GF, Migaldi M, Marchegiano P, Rumpianesi F, Ferrari F (2013) Serratia marcescens in a neonatal intensive care unit: two long-term multiclone outbreaks in a 10-year observational study. New Microbiol 36(4):373–383

    PubMed  CAS  Google Scholar 

  8. Cilieborg MS, Boye M, Sangild PT (2012) Bacterial colonization and gut development in preterm neonates. Early Hum Dev 88(Supplement 1):S41–S49

    Article  PubMed  Google Scholar 

  9. Clarivet B, Grau D, Jumas-Bilak E, Jean-Pierre H, Pantel A, Parer S, Lotthé A (2016) Persisting transmission of carbapenemase producing Klebsiella pneumoniae due to an environmental reservoir in a university hospital, France, 2012 to 2014. Euro Surveill 21(17). https://doi.org/10.2807/1560-7917.ES.2016.21.17.30213

  10. Creamer E, Humphreys H (2008) The contribution of beds to healthcare-associated infection: the importance of adequate decontamination. J Hosp Infect 69(1):8–23

    Article  PubMed  CAS  Google Scholar 

  11. Dalben M, Varkulja G, Basso M, Krebs VLJ, Gibelli MA, van der Heijden I, Rossi F, Duboc G, Levin AS, Costa SF (2008) Investigation of an outbreak of Enterobacter cloacae in a neonatal unit and review of the literature. J Hosp Infect 70(1):7–14

    Article  PubMed  CAS  Google Scholar 

  12. Dancer SJ (2014) Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev 27(4):665–690

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  13. de Goffau MC, Bergman KA, de Vries HJ et al (2011) Cold spots in neonatal incubators are hot spots for microbial contamination. Appl Environ Microbiol 77(24):8568–8572

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  14. de Oliveira AC, Viana REH, Damasceno QS (2012) Contamination of hospital mattresses by microorganisms of epidemiological relevance: an integrative review. J Nurs UFPE on line 7(1):236–245

    Google Scholar 

  15. Denkel LA, Schwab F, Kola A, Leistner R, Garten L, von Weizsacker K, Geffers C, Gastmeier P, Piening B (2014) The mother as most important risk factor for colonization of very low birth weight (VLBW) infants with extended-spectrum β-lactamase producing Enterobacteriaceae (ESBL-E). J Antimicrob Chemother 69(8):2230–2237

    Article  PubMed  CAS  Google Scholar 

  16. Dubois V, De Barbeyrac B, Rogues A-M et al (2010) CTX-M-producing Escherichia coli in a maternity ward: a likely community importation and evidence of mother-to-neonate transmission. J Antimicrob Chemother 65(7):1368–1371

    Article  PubMed  CAS  Google Scholar 

  17. Dziri D, Klibi N, Alonso CA, Ben Said L et al (2016) Characterization of extended-spectrum β-lactamase (ESBL)-producing Klebsiella, Enterobacter, and Citrobacter obtained in environmental samples of a Tunisian hospital. Diagn Microbiol Infect Dis 86(2):190–193

    Article  PubMed  CAS  Google Scholar 

  18. Fabbri G, Panico M, Dallolio L, Suzzi R, Ciccia M, Sandri F, Farruggia P (2013) Outbreak of ampicillin/piperacillin-resistant Klebsiella pneumoniae in a neonatal intensive care unit (NICU): investigation and control measures. Int J Environ Res Public Health 10(3):808–815

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  19. Gallimore CI, Taylor C, Gennery AR, Cant AJ, Galloway A, Xerry J, Adigwe J, Gray JJ (2008) Contamination of the hospital environment with gastroenteric viruses: comparison of two pediatric wards over a winter season. J Clin Microbiol 46(9):3112–3115

    Article  PubMed  PubMed Central  Google Scholar 

  20. Golan Y, Doron S, Sullivan B, Snydman DR (2005) Transmission of vancomycin-resistant Enterococcus in a neonatal intensive care unit. Pediatr Infect Dis J 24(6):566–567

    Article  PubMed  Google Scholar 

  21. Gouby A, Neuwirth C, Bourg G, Bouziges N, Carles-Nurit MJ, Despaux E, Ramuz M (1994) Epidemiological study by pulsed-field gel electrophoresis of an outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae in a geriatric hospital. J Clin Microbiol 32(2):301–305

    PubMed  CAS  PubMed Central  Google Scholar 

  22. Griffith CJ, Dancer SJ (2009) Hospital cleaning: problems with steam cleaning and microfibre. J Hosp Infect 72(4):360–361

    Article  PubMed  CAS  Google Scholar 

  23. Gupta A (2002) Hospital-acquired infections in the neonatal intensive care unit-Klebsiella pneumoniae. Semin Perinatol 26(5):340–345

    Article  PubMed  Google Scholar 

  24. Hartz LE, Bradshaw W, Brandon DH (2015) Potential NICU environmental influences on the neonate’s microbiome: a systematic review. Adv Neonatal Care 15(5):324–335

    Article  PubMed  PubMed Central  Google Scholar 

  25. Health C for D and R. Safety Communications - Damaged or Worn Covers for Medical Bed Mattresses Pose Risk of Contamination and Patient Infection: FDA Safety Communication. Available at: http://www.fda.gov/MedicalDevices/Safety/AlertsandNotices/ucm348016.htm. Accessed 12 Nov 2016

  26. Hendrik TC, Voor in ‘t holt AF, Vos MC (2015) Clinical and molecular epidemiology of extended-spectrum beta-lactamase-producing Klebsiella spp.: a systematic review and meta-analyses. PLoS One 10(10):e0140754

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  27. Hosein IK, Hoffman PN, Ellam S, Asseez TM, Fakokunde A, Silles J, Devereux E, Kaur D, Bosanquet J (2013) Summertime Bacillus cereus colonization of hospital newborns traced to contaminated, laundered linen. J Hosp Infect 85(2):149–154

    Article  PubMed  CAS  Google Scholar 

  28. Lin R, Wu B, Xu X-F, Liu X-C, Ye H, Ye GY (2012) Extended-spectrum beta-lactamase-producing Klebsiella pneumoniae infection in a neonatal intensive care unit. World J Pediatr 8(3):268–271

    Article  PubMed  CAS  Google Scholar 

  29. Macdonald TM, Langley JM, Mailman T et al (2011) Serratia marcescens outbreak in a neonatal intensive care unit related to the exit port of an oscillator. Pediatr Crit Care Med 12(6):e282–e286

    Article  PubMed  Google Scholar 

  30. Madani TA, Alsaedi S, James L, Eldeek BS, Jiman-Fatani AA, Alawi MM, Marwan D, Cudal M, Macapagal M, Bahlas R, Farouq M (2011) Serratia marcescens-contaminated baby shampoo causing an outbreak among newborns at King Abdulaziz University Hospital, Jeddah, Saudi Arabia. J Hosp Infect 78(1):16–19

    Article  PubMed  CAS  Google Scholar 

  31. Nakamura K, Kaneko M, Abe Y, Yamamoto N, Mori H, Yoshida A, Ohashi K, Miura S, Yang TT, Momoi N, Kanemitsu K (2016) Outbreak of extended-spectrum β-lactamase producing Escherichia coli transmitted through breast milk sharing in a neonatal intensive care unit. J Hosp Infect 92(1):42–46

    Article  PubMed  CAS  Google Scholar 

  32. Narayan SA, Kool JL, Vakololoma M, Steer AC, Mejia A, Drake A, Jenney A, Turton JF, Kado J, Tikoduadua L (2009) Investigation and control of an outbreak of Enterobacter aerogenes bloodstream infection in a neonatal intensive care unit in Fiji. Infect Control Hosp Epidemiol 30(8):797–800

    Article  PubMed  Google Scholar 

  33. Pessoa-Silva CL, Meurer Moreira B, Câmara Almeida V, Flannery B, Almeida Lins MC, Mello Sampaio JL, Martins Teixeira L, Vaz Miranda LE, Riley LW, Gerberding JL (2003) Extended-spectrum β-lactamase-producing Klebsiella pneumoniae in a neonatal intensive care unit: risk factors for infection and colonization. J Hosp Infect 53(3):198–206

    Article  PubMed  CAS  Google Scholar 

  34. Pestourie N, Garnier F, Barraud O, Bedu A, Ploy MC, Mounier M (2014) Outbreak of AmpC β-lactamase-hyper-producing Enterobacter cloacae in a neonatal intensive care unit in a French teaching hospital. Am J Infect Control 42(4):456–458

    Article  PubMed  Google Scholar 

  35. Rastogi V, Nirwan PS, Jain S, Kapil A (2010) Nosocomial outbreak of septicaemia in neonatal intensive care unit due to extended spectrum β-lactamase producing Klebsiella pneumoniae showing multiple mechanisms of drug resistance. Indian J Med Microbiol 28(4):380–384

    Article  PubMed  CAS  Google Scholar 

  36. Romano-Bertrand S, Filleron A, Mesnage R, Lotthé A, Didelot M, Burgel L, Bilak E, Cambonie G, Parer S (2014) Staphylococcus aureus in a neonatal care center: methicillin-susceptible strains should be a main concern. Antimicrob Resist Infect Control 3:21

    Article  PubMed  PubMed Central  Google Scholar 

  37. Sexton JD, Tanner BD, Maxwell SL, Gerba CP (2011) Reduction in the microbial load on hightouch surfaces in hospital rooms by treatment with a portable saturated steam vapor disinfection system. Am J Infect Control 39(8):655–662

    Article  PubMed  Google Scholar 

  38. Vonberg RP, Weitzel-Kage D, Behnke M, Gastmeier P (2011) Worldwide outbreak database: the largest collection of nosocomial outbreaks. Infection 39(1):29–34

    Article  PubMed  Google Scholar 

  39. Yu M, Cross K, Petrich A, Fish J (2016) Crib mattress investigation: a quality improvement study to assess mattress cover permeability and bacterial growth in crib mattresses. Am J Infect Control 44(7):837–839

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the University Hospital of Montpellier and the association ADEREMPHA, Sauzet, France.

Author information

Authors and Affiliations

  1. Département d’Hygiène Hospitalière, CHU Montpellier, Montpellier, France

    Lucile Cadot & Hélène Bruguière

  2. Hydrosciences Montpellier, IRD, CNRS, Univ Montpellier, Département d’Hygiène Hospitalière, CHU Montpellier, 15 avenue Charles Flahault, BP 14491, 34093, Montpellier cedex 5, France

    Estelle Jumas-Bilak, Sylvie Parer & Sara Romano-Bertrand

  3. Laboratoire de Bacteriologie, CHU Montpellier, Montpellier, France

    Marie-Noëlle Didelot

  4. Hydrosciences Montpellier, IRD, CNRS, Univ Montpellier, Montpellier, France

    Agnès Masnou

  5. Pharmacie à Usage Interieur, CHU Montpellier, Montpellier, France

    Gaëlle de Barry

  6. Service de Néonatologie, CHU Montpellier, Montpellier, France

    Gilles Cambonie

Authors
  1. Lucile Cadot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hélène Bruguière
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Estelle Jumas-Bilak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marie-Noëlle Didelot
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Agnès Masnou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gaëlle de Barry
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gilles Cambonie
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sylvie Parer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sara Romano-Bertrand
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LC wrote the first draft of the manuscript and provided environmental sampling and bacteriological analyses; HB made the audit observations and analyzed their results; EJB helped for the interpretation of results from bacteriological analyses; MND contributed to the survey of cases in the NCC wards; AM performed molecular typing on strains; GDB provided antibiotic consumption reports; GC diagnosed cases and contributed to their survey in the NCC wards; SP managed the audit study and the application of preventive measures; SRB managed the environmental investigation, the application of preventive measures, and the writing of the manuscript. All authors have seen and approved the submission of this version of the manuscript and take full responsibility for the manuscript. No authors received any grant or honorarium or payment for producing this manuscript.

Corresponding author

Correspondence to Sara Romano-Bertrand.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.

Additional information

Communicated by Patrick Van Reempts

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 84 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cadot, L., Bruguière, H., Jumas-Bilak, E. et al. Extended spectrum beta-lactamase-producing Klebsiella pneumoniae outbreak reveals incubators as pathogen reservoir in neonatal care center. Eur J Pediatr 178, 505–513 (2019). https://doi.org/10.1007/s00431-019-03323-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00431-019-03323-w

Keywords

Search

Navigation