A survey on practices for active surveillance of carriage of multidrug-resistant bacteria in hospitals in the Autonomous Community of Valencia, Spain

  • Nuria Tormo
  • Eliseo Albert
  • Emilio Borrajo
  • Monserrat Bosque
  • Juan José Camarena
  • Victoria Domínguez
  • Encarnación Fuentes
  • Isabel Gascón
  • Bárbara Gomila
  • Nieves Gonzalo
  • Marta Jiménez
  • Olalla Martínez
  • José Miguel Nogueira
  • Nieves Orta
  • Josep Prat
  • Juan Carlos Rodríguez
  • Concepción Gimeno
  • David NavarroEmail author
  • on behalf of the Working Group of the Autonomous Community of Valencia (ACV) for Optimization of Microbiological Diagnostic Processes
Original Article


A questionnaire-based cross-sectional study was conducted to gather information on current microbiological practices for active surveillance of carriage of multidrug-resistant (MDR) bacteria in hospitals from 14 health departments of the Autonomous Community of Valencia (ACV), Spain, which together provided medical attention to 3,271,077 inhabitants in 2017, approximately 70% of the population of the ACV. The survey consisted of 35 questions on MDR bacteria screening policies, surveillance approach chosen (universal vs. targeted), and microbiological methods and processes in use for routine detection and reporting of colonization by MDR bacteria, including the anatomical sites scheduled to be sampled for each MDR bacterial species, and the methodology employed (culture-based, molecular-based, or both). Our study revealed striking differences across centers, likely attributable to the lack of consensus on optimal protocols for sampling, body sites for screening, and microbiological testing, thus underscoring the need for consensus guidelines on these issues.


Multidrug-resistant (MDR) bacteria Surveillance cultures Chromogenic agar media Molecular testing MDR bacteria transmission 



We thank Merck Sharp & Dohme (MSD) for organizing the meeting logistics of the Working Group of the Autonomous Community of Valencia (ACV) for Optimization of Microbiological Diagnostic Processes.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

The ethical committee of the participating hospitals deemed specific approval for this study unnecessary.

Informed consent

Not applicable (as discussed with the institutional medical ethical committee).

Supplementary material

10096_2018_3340_MOESM1_ESM.doc (310 kb)
ESM 1 (DOC 310 kb)


  1. 1.
    Spellberg B, Blaser M, Guidos RJ, Boucher HW, Bradley JS, Eisenstein BI, Gerding D, Lynfield R, Reller LB, Rex J, Schwartz D, Septimus E, Tenover FC, Gilbert DN (2011) Combating antimicrobial resistance: policy recommendations to save lives. Clin Infect Dis 52(Suppl 5):S397–S428PubMedGoogle Scholar
  2. 2.
    Peleg AY, Hooper DC (2010) Hospital-acquired infections due to Gram-negative bacteria. N Engl J Med 362:1804–1813CrossRefGoogle Scholar
  3. 3.
    Mauldin PD, Salgado CD, Hansen IS, Durup DT, Bosso JA (2010) Attributable hospital cost and length of stay associated with health care-associated infections caused by antibiotic-resistant gram-negative bacteria. Antimicrob Agents Chemother 54:109–115CrossRefGoogle Scholar
  4. 4.
    Vardakas KZ, Rafailidis PI, Konstantelias AA, Falagas ME (2013) Predictors of mortality in patients with infections due to multi-drug resistant Gram negative bacteria: the study, the patient, the bug or the drug? J Inf Secur 66:401–414Google Scholar
  5. 5.
    Gupta N, Limbago BM, Patel JB, Kallen AJ (2011) Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis 53:60–67CrossRefGoogle Scholar
  6. 6.
    Coia JE, Duckworth GJ, Edwards DI, Fry C, Humphreys H, Mallaghan C, Tucker DR (2006) Guidelines for the control and prevention of meticillin resistant Staphylococcus aureus (MRSA) in healthcare facilities. J Hosp Infect 63(Suppl 1):S1e44Google Scholar
  7. 7.
    Otter JA, Mutters NT, Tacconelli E, Gikas A, Holmes AH (2015) Controversies in guidelines for the control of multidrug-resistant Gram-negative bacteria in EU countries. Clin Microbiol Infect 21:1057–1066CrossRefGoogle Scholar
  8. 8.
    Tacconelli E, Cataldo MA, Dancer SJ, De Angelis G, Falcone M, Frank U, Kahlmeter G, Pan A, Petrosillo N, Rodríguez-Baño J, Singh N, Venditti M, Yokoe DS, Cookson B (2014) ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients. Clin Microbiol Infect 20(Suppl. 1):1–55CrossRefGoogle Scholar
  9. 9.
    Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–281CrossRefGoogle Scholar
  10. 10.
    Kock R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, Mielke M, Peters G, Skov RL, Struelens MJ, Tacconelli E, Witte W, Friedrich AW (2014) Systematic literature analysis and review of targeted preventive measures to limit healthcare-associated infections by meticillin-resistant Staphylococcus aureus. Euro Surveill 19(29)Google Scholar
  11. 11.
    ECDC European Centre for Disease Prevention and Control (2014) Systematic review of the effectiveness of infection control measures to prevent the transmission of carbapenemase-producing Enterobacteriaceae through cross-border transfer of patients. ECDC, StockholmGoogle Scholar
  12. 12.
    Royal College of Physicians of Ireland (2012) Guidelines for the prevention and control of multi-drug resistant organisms (MDRO) excluding MRSA in the healthcare setting. Accessed 13 June 2018
  13. 13.
    Public Health England (2013) Acute trust toolkit for the early detection, management and control of carbapenemase-producing Enterobacteriaceae. Accessed 13 June 2018
  14. 14.
    Health Protection Scotland (2013) Carbapenemase producing Enterobacteriaceae (CPE) prevention and management toolkit for inpatient areas. Accessed 13 June 2018
  15. 15.
    Magiorakos AP, Burns K, Rodríguez Baño J, Borg M, Daikos G, Dumpis U, Lucet JC, Moro ML, Tacconelli E, Simonsen GS, Szilágyi E, Voss A, Weber JT (2017) Infection prevention and control measures and tools for the prevention of entry of carbapenem-resistant Enterobacteriaceae into healthcare settings: guidance from the European Centre for Disease Prevention and Control. Antimicrob Resist Infect Control 6:113CrossRefGoogle Scholar
  16. 16.
    Lapointe-Shaw L, Voruganti T, Kohler P, Thein HH, Sander B, McGeer A (2017) Cost-effectiveness analysis of universal screening for carbapenemase-producing Enterobacteriaceae in hospital inpatients. Eur J Clin Microbiol Infect Dis 36:1047–1055CrossRefGoogle Scholar
  17. 17.
    Otter JA, Dyakova E, Bisnauthsing KN, Querol-Rubiera A, Patel A, Ahanonu C, Tosas Auguet O, Edgeworth JD, Goldenberg SD (2016) Universal hospital admission screening for carbapenemase-producing organisms in a low-prevalence setting. J Antimicrob Chemother 71:3556–3561CrossRefGoogle Scholar
  18. 18.
    Richter SS, Marchaim D (2017) Screening for carbapenem-resistant Enterobacteriaceae: who, when, and how? Virulence 8:417–442CrossRefGoogle Scholar
  19. 19.
    Kardaś-Słoma L, Lucet JC, Perozziello A, Pelat C, Birgand G, Ruppé E, Boëlle PY, Andremont A, Yazdanpanah Y (2017) Universal or targeted approach to prevent the transmission of extended-spectrum beta-lactamase-producing Enterobacteriaceae in intensive care units: a cost-effectiveness analysis. BMJ Open 7:e017402CrossRefGoogle Scholar
  20. 20.
    Ho KW, Ng WT, Ip M, You JH (2016) Active surveillance of carbapenem-resistant Enterobacteriaceae in intensive care units: is it cost-effective in a nonendemic region? Am J Infect Control 44:394–399CrossRefGoogle Scholar
  21. 21.
    Gazin M, Paasch F, Goossens H, Malhotra-Kumar S (2012) Current trends in culture-based and molecular detection of extended-spectrum-β-lactamase-harboring and carbapenem-resistant Enterobacteriaceae. J Clin Microbiol 50:1140–1146CrossRefGoogle Scholar
  22. 22.
    Viau R, Frank KM, Jacobs MR, Wilson B, Kaye K, Donskey CJ, Perez F, Endimiani A, Bonomo RA (2016) Intestinal carriage of carbapenemase-producing organisms: current status of surveillance methods. Clin Microbiol Rev 29:1–27CrossRefGoogle Scholar
  23. 23.
    García-Fernández S, Hernández-García M, Valverde A, Ruiz-Garbajosa P, Morosini MI, Cantón R (2017) CHROMagar mSuperCARBA performance in carbapenem-resistant Enterobacteriaceae isolates characterized at molecular level and routine surveillance rectal swab specimens. Diagn Microbiol Infect Dis 87:207–209CrossRefGoogle Scholar
  24. 24.
    Ciesielczuk H, Phee LM, Dolphin H, Wilks M, Cherian BP, Wareham DW (2018) Optimal detection of carbapenemase-producing Enterobacteriaceae from rectal samples: a role for enrichment? J Hosp Infect 98:270–274CrossRefGoogle Scholar
  25. 25.
    Wu PJ, Jeyaratnam D, Tosas O, Cooper BS, French G (2017) Point-of-care universal screening for meticillin-resistant Staphylococcus aureus: a cluster-randomized cross-over trial. J Hosp Infect 95:245–252CrossRefGoogle Scholar
  26. 26.
    Derde LPG, Cooper BS, Goossens H, Malhotra-Kumar S, Willems RJL, Gniadkowski M, Hryniewicz W, Empel J, Dautzenberg MJD, Annane D, Aragão I, Chalfine A, Dumpis U, Esteves F, Giamarellou H, Muzlovic I, Nardi G, Petrikkos GL, Tomic V, Martí AT, Stammet P, Brun-Buisson C, Bonten MJM, MOSAR WP3 Study Team (2014) Interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in intensive care units: an interrupted time series study and cluster randomised trial. Lancet Infect Dis 14:31–39CrossRefGoogle Scholar
  27. 27.
    Oteo J, Bou G, Chaves F, Oliver A (2017) Microbiological methods for surveillance of carrier status of multiresistant bacteria. Enferm Infecc Microbiol Clin 35:667–675CrossRefGoogle Scholar
  28. 28.
    van den Bijllaardt W, Janssens MM, Buiting AG, Muller AE, Mouton JW, Verweij JJ (2018) Extended-spectrum β-lactamase (ESBL) polymerase chain reaction assay on rectal swabs and enrichment broth for detection of ESBL carriage. J Hosp Infect 98:264–269CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Nuria Tormo
    • 1
  • Eliseo Albert
    • 2
  • Emilio Borrajo
    • 3
  • Monserrat Bosque
    • 4
  • Juan José Camarena
    • 5
  • Victoria Domínguez
    • 4
  • Encarnación Fuentes
    • 6
  • Isabel Gascón
    • 7
  • Bárbara Gomila
    • 8
  • Nieves Gonzalo
    • 9
  • Marta Jiménez
    • 10
  • Olalla Martínez
    • 11
  • José Miguel Nogueira
    • 5
  • Nieves Orta
    • 12
  • Josep Prat
    • 13
  • Juan Carlos Rodríguez
    • 14
  • Concepción Gimeno
    • 1
  • David Navarro
    • 2
    Email author
  • on behalf of the Working Group of the Autonomous Community of Valencia (ACV) for Optimization of Microbiological Diagnostic Processes
  1. 1.Microbiology ServiceConsorcio Hospital General UniversitarioValenciaSpain
  2. 2.Microbiology Service, and Department of Microbiology, School of MedicineHospital Clínico UniversitarioValenciaSpain
  3. 3.Microbiology UnitHospital Vega BajaOrihuelaSpain
  4. 4.Microbiology ServiceHospital Arnau de VilanovaValenciaSpain
  5. 5.Hospital Universitario Dr. PesetValenciaSpain
  6. 6.Microbiology UnitHospital Virgen de los LiriosAlcoiSpain
  7. 7.Hospital General UniversitarioEldaSpain
  8. 8.Microbiology ServiceHospital General UniversitarioCastellonSpain
  9. 9.Microbiology ServiceHospital General UniversitarioElcheSpain
  10. 10.Microbiology Unit, Hospital ManisesManisesSpain
  11. 11.Hospital Universitario de la RiberaAlziraSpain
  12. 12.Microbiology Unit, Hospital Francesc de BorjaGandiaSpain
  13. 13.Microbiology UnitHospital de SaguntoValenciaSpain
  14. 14.Hospital General UniversitarioAlicanteSpain

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