Research Open Access
Like 0



Increasing resistance to antibiotics poses medical challenges worldwide. Prospective data on carriage prevalence of multidrug resistant organisms (MDRO) in children at hospital admission are limited and associated risk factors are poorly defined.


To determine prevalence of MDRO carriage in children at admission to our paediatric hospital in Hamburg and to identify MDRO carriage risk factors.


We prospectively obtained and cultured nasal/throat and inguinal/anal swabs from children (≤ 18 years) at admission between September 2018 and May 2019 to determine prevalence of meticillin-resistant (MRSA), multidrug-resistant Gram-negative bacteria (MRGN) and vancomycin-resistant enterococcus (VRE) and associated species. We collected medical histories using a questionnaire and evaluated 31 risk factors using logistic regression models.


MDRO carriage prevalence of 3,964 children was 4.31% (95% confidence interval (CI): 3.69–5.00). MRSA carriage prevalence was 0.68% (95% CI: 0.44–0.99), MRGN prevalence was 3.64% (95% CI: 3.07–4.28) and VRE prevalence 0.08% (95% CI: 0.02–0.22). MDRO carriage was associated with MRGN history (odds ratio (OR): 6.53; 95% CI: 2.58–16.13), chronic condition requiring permanent care (OR: 2.67; 95% CI: 1.07–6.13), antibiotic therapy (OR: 1.92, 95% CI: 1.24–2.94), living in a care facility (OR: 3.34; 95% CI: 0.72–12.44) and refugee status in previous 12 months (OR: 1.91; 95% CI: 0.27–8.02). Compared to established practice, screening using risk-factors had better diagnostic sensitivity (86.13%; 95% CI: 80.89–91.40) and specificity (73.54%; 95% CI: 72.12–74.97).


MRGN carriage was higher than MRSA and VRE. Extended risk-factor-based admission screening system seems warranted.


Article metrics loading...

Loading full text...

Full text loading...



  1. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, Simonsen GS, et al. , Burden of AMR Collaborative Group. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis. 2019;19(1):56-66.  https://doi.org/10.1016/S1473-3099(18)30605-4  PMID: 30409683 
  2. van den Bunt G, van Pelt W, Hidalgo L, Scharringa J, de Greeff SC, Schürch AC, et al. Prevalence, risk factors and genetic characterisation of extended-spectrum beta-lactamase and carbapenemase-producing Enterobacteriaceae (ESBL-E and CPE): a community-based cross-sectional study, the Netherlands, 2014 to 2016. Euro Surveill. 2019;24(41):1800594.  https://doi.org/10.2807/1560-7917.ES.2019.24.41.1800594  PMID: 31615600 
  3. Walter J, Noll I, Feig M, Weiss B, Claus H, Werner G, et al. Decline in the proportion of methicillin resistance among Staphylococcus aureus isolates from non-invasive samples and in outpatient settings, and changes in the co-resistance profiles: an analysis of data collected within the Antimicrobial Resistance Surveillance Network, Germany 2010 to 2015. BMC Infect Dis. 2017;17(1):169.  https://doi.org/10.1186/s12879-017-2271-6  PMID: 28231850 
  4. Gijón M, Bellusci M, Petraitiene B, Noguera-Julian A, Zilinskaite V, Sanchez Moreno P, et al. Factors associated with severity in invasive community-acquired Staphylococcus aureus infections in children: a prospective European multicentre study. Clin Microbiol Infect. 2016;22(7):643.e1-6.  https://doi.org/10.1016/j.cmi.2016.04.004  PMID: 27107685 
  5. Sutter DE, Milburn E, Chukwuma U, Dzialowy N, Maranich AM, Hospenthal DR. Changing Susceptibility of Staphylococcus aureus in a US Pediatric Population. Pediatrics. 2016;137(4):e20153099.  https://doi.org/10.1542/peds.2015-3099  PMID: 26933211 
  6. Martischang R, Buetti N, Balmelli C, Saam M, Widmer A, Harbarth S. Nation-wide survey of screening practices to detect carriers of multi-drug resistant organisms upon admission to Swiss healthcare institutions. Antimicrob Resist Infect Control. 2019;8(1):37.  https://doi.org/10.1186/s13756-019-0479-5  PMID: 30809380 
  7. van Bijnen EM, Paget J, de Lange-de Klerk ES, den Heijer CD, Versporten A, Stobberingh EE, et al. , collaboration with the APRES Study Team. Antibiotic Exposure and Other Risk Factors for Antimicrobial Resistance in Nasal Commensal Staphylococcus aureus: An Ecological Study in 8 European Countries. PLoS One. 2015;10(8):e0135094.  https://doi.org/10.1371/journal.pone.0135094  PMID: 26262679 
  8. Johnson K, Frei R, Heininger U. Prospective, cross-sectional study on MSSA and MRSA colonisation in hospitalised children. Eur J Pediatr. 2015;174(9):1255-62.  https://doi.org/10.1007/s00431-015-2606-5  PMID: 26272252 
  9. Huebner NO, Dittmann K, Henck V, Wegner C, Kramer A, Action Group Infection Prevention (AGIP). Epidemiology of multidrug resistant bacterial organisms and Clostridium difficile in German hospitals in 2014: Results from a nationwide one-day point prevalence of 329 German hospitals. BMC Infect Dis. 2016;16(1):467.  https://doi.org/10.1186/s12879-016-1756-z  PMID: 27590879 
  10. Skjøt-Arkil H, Mogensen CB, Lassen AT, Johansen IS, Chen M, Petersen P, et al. Carrier prevalence and risk factors for colonisation of multiresistant bacteria in Danish emergency departments: a cross-sectional survey. BMJ Open. 2019;9(6):e029000.  https://doi.org/10.1136/bmjopen-2019-029000  PMID: 31253624 
  11. Bouchiat C, Curtis S, Spiliopoulou I, Bes M, Cocuzza C, Codita I, et al. , ESCMID Study Group on Staphylococci and Staphylococcal Infections (ESGS). MRSA infections among patients in the emergency department: a European multicentre study. J Antimicrob Chemother. 2017;72(2):372-5.  https://doi.org/10.1093/jac/dkw431  PMID: 27798212 
  12. Stoliaroff-Pépin A, Arvand M, Mielke M. Bericht zum Treffen der Moderatoren der regionalen MRENetzwerke am Robert Koch-Institut. [Report on the meeting of the moderators of the regional MDRO networks at the Robert Koch Institute]. Epidemiologisches Bulletin. 12 Oct 2017. German. Available from: https://edoc.rki.de/bitstream/handle/176904/2846/2377H38MG2d1U.pdf?sequence=1&isAllowed=y
  13. Islam S, Selvarangan R, Kanwar N, McHenry R, Chappell JD, Halasa N, et al. Intestinal Carriage of Third-Generation Cephalosporin-Resistant and Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae in Healthy US Children. J Pediatric Infect Dis Soc. 2018;7(3):234-40.  https://doi.org/10.1093/jpids/pix045  PMID: 28992133 
  14. Hamprecht A, Rohde AM, Behnke M, Feihl S, Gastmeier P, Gebhardt F, et al. , DZIF-ATHOS Study Group. Colonization with third-generation cephalosporin-resistant Enterobacteriaceae on hospital admission: prevalence and risk factors. J Antimicrob Chemother. 2016;71(10):2957-63.  https://doi.org/10.1093/jac/dkw216  PMID: 27317445 
  15. Otter JA, Herdman MT, Williams B, Tosas O, Edgeworth JD, French GL. Low prevalence of meticillin-resistant Staphylococcus aureus carriage at hospital admission: implications for risk-factor-based vs universal screening. J Hosp Infect. 2013;83(2):114-21.  https://doi.org/10.1016/j.jhin.2012.10.008  PMID: 23313028 
  16. Gesualdo F, Bongiorno D, Rizzo C, Bella A, Menichella D, Stefani S, et al. MRSA nasal colonization in children: prevalence meta-analysis, review of risk factors and molecular genetics. Pediatr Infect Dis J. 2013;32(5):479-85.  https://doi.org/10.1097/INF.0b013e3182864e4c  PMID: 23340553 
  17. Rohde AM, Zweigner J, Wiese-Posselt M, Schwab F, Behnke M, Kola A, et al. Prevalence of third-generation cephalosporin-resistant Enterobacterales colonization on hospital admission and ESBL genotype-specific risk factors: a cross-sectional study in six German university hospitals. J Antimicrob Chemother. 2020;75(6):1631-8.  https://doi.org/10.1093/jac/dkaa052  PMID: 32173738 
  18. Grundmann H, Glasner C, Albiger B, Aanensen DM, Tomlinson CT, Andrasević AT, et al. , European Survey of Carbapenemase-Producing Enterobacteriaceae (EuSCAPE) Working Group. Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): a prospective, multinational study. Lancet Infect Dis. 2017;17(2):153-63.  https://doi.org/10.1016/S1473-3099(16)30257-2  PMID: 27866944 
  19. Otter JA, Natale A, Batra R, Tosas Auguet O, Dyakova E, Goldenberg SD, et al. Individual- and community-level risk factors for ESBL Enterobacteriaceae colonization identified by universal admission screening in London. Clin Microbiol Infect. 2019;25(10):1259-65.  https://doi.org/10.1016/j.cmi.2019.02.026  PMID: 30849431 
  20. Fulchini R, Albrich WC, Kronenberg A, Egli A, Kahlert CR, Schlegel M, et al. Antibiotic-resistant pathogens in different patient settings and identification of surveillance gaps in Switzerland - a systematic review. Epidemiol Infect. 2019;147:e259.  https://doi.org/10.1017/S0950268819001523  PMID: 31466538 
  21. Peters C, Dulon M, Kleinmüller O, Nienhaus A, Schablon A. MRSA Prevalence and Risk Factors among Health Personnel and Residents in Nursing Homes in Hamburg, Germany - A Cross-Sectional Study. PLoS One. 2017;12(1):e0169425.  https://doi.org/10.1371/journal.pone.0169425  PMID: 28068356 
  22. Simon A, Tenenbaum T. Surveillance of multidrug-resistant Gram-negative pathogens in high-risk neonates--does it make a difference? Pediatr Infect Dis J. 2013;32(4):407-9.  https://doi.org/10.1097/INF.0b013e3182875227  PMID: 23340567 
  23. Wegner C, Hübner NO, Gleich S, Thalmaier U, Krüger CM, Kramer A. One-day point prevalence of emerging bacterial pathogens in a nationwide sample of 62 German hospitals in 2012 and comparison with the results of the one-day point prevalence of 2010. GMS Hyg Infect Control. 2013;8(1):Doc12. PMID: 23967398 
  24. Arya R, Antonisamy B, Kumar S. Sample size estimation in prevalence studies. Indian J Pediatr. 2012;79(11):1482-8.  https://doi.org/10.1007/s12098-012-0763-3  PMID: 22562262 
  25. Pourhoseingholi MA, Vahedi M, Rahimzadeh M. Sample size calculation in medical studies. Gastroenterol Hepatol Bed Bench. 2013;6(1):14-7. PMID: 24834239 
  26. Clopper CJ, Pearson ES. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika. 1934;26(4):404-13.  https://doi.org/10.1093/biomet/26.4.404 
  27. Lauritsen J, Bruus M. EpiData: A Comprehensive Tool for Validated Entry and Documentation of Data Version 3. Odense, Denmark: The Epi Data Association. 2003. http://www.epidata.dk/
  28. Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, et al. Welcome to the tidyverse. J Open Source Softw. 2019;4(43):1686.  https://doi.org/10.21105/joss.01686 
  29. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. 2021. https://www.R-project.org/
  30. Kaarme J, Riedel H, Schaal W, Yin H, Nevéus T, Melhus Å. Rapid increase in carriage rates of Enterobacteriaceae producing extended-spectrum β-lactamases in healthy preschool children, Sweden. Emerg Infect Dis. 2018;24(10):1874-81.  https://doi.org/10.3201/eid2410.171842  PMID: 30226162 
  31. van den Bunt G, Liakopoulos A, Mevius DJ, Geurts Y, Fluit AC, Bonten MJ, et al. ESBL/AmpC-producing Enterobacteriaceae in households with children of preschool age: prevalence, risk factors and co-carriage. J Antimicrob Chemother. 2017;72(2):589-95.  https://doi.org/10.1093/jac/dkw443  PMID: 27789683 
  32. Wolfensberger A, Kuster SP, Marchesi M, Zbinden R, Hombach M. The effect of varying multidrug-resistence (MDR) definitions on rates of MDR gram-negative rods. Antimicrob Resist Infect Control. 2019;8(1):193.  https://doi.org/10.1186/s13756-019-0614-3  PMID: 31798839 
  33. European Centre for Disease Prevention and Control (ECDC). Surveillance of antimicrobial resistance in Europe: annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 2017. Stockholm: ECDC; 15 Nov 2018. Available from: https://www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-resistance-europe-2017
  34. Roope LSJ, Smith RD, Pouwels KB, Buchanan J, Abel L, Eibich P, et al. The challenge of antimicrobial resistance: What economics can contribute. Science. 2019;364(6435):eaau4679.  https://doi.org/10.1126/science.aau4679  PMID: 30948524 
  35. Saporito L, Graziano G, Mescolo F, Amodio E, Insinga V, Rinaudo G, et al. Efficacy of a coordinated strategy for containment of multidrug-resistant Gram-negative bacteria carriage in a Neonatal Intensive Care Unit in the context of an active surveillance program. Antimicrob Resist Infect Control. 2021;10(1):30.  https://doi.org/10.1186/s13756-021-00902-1  PMID: 33541419 
  36. Wielders CCH, Van Duijkeren E, Van Den Bunt G, Meijs AP, Dierikx CM, Bonten MJM, et al. Seasonality in carriage of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in the general population: a pooled analysis of nationwide cross-sectional studies. Epidemiol Infect. 2020;148:e68.  https://doi.org/10.1017/S0950268820000539  PMID: 32081112 
  37. Reinheimer C, Abdollahi P, Zacharowski K, Meybohm P, Mutlak H, Klingebiel T, et al. Prevalence of multidrug-resistant organisms in refugee patients admitted to a German university hospital depending on duration of stay in Germany. GMS Hyg Infect Control. 2019;14:Doc07. PMID: 31293878 
  38. de Lastours V, Malosh RE, Aiello AE, Foxman B. Prevalence of Escherichia coli carriage in the oropharynx of ambulatory children and adults with and without upper respiratory symptoms. Ann Am Thorac Soc. 2015;12(3):461-3.  https://doi.org/10.1513/AnnalsATS.201412-586LE  PMID: 25786154 
  39. Makhoul IR, Sujov P, Smolkin T, Lusky A, Reichman B, Israel Neonatal Network. Pathogen-specific early mortality in very low birth weight infants with late-onset sepsis: a national survey. Clin Infect Dis. 2005;40(2):218-24.  https://doi.org/10.1086/426444  PMID: 15655738 
  40. Tenenbaum T, Becker K-P, Lange B, Martin A, Schäfer P, Weichert S, et al. Prevalence of multidrug-resistant organisms in hospitalized pediatric refugees in an University Children’s Hospital in Germany 2015–2016. Infect Control Hosp Epidemiol. 2016;37(11):1310-4.  https://doi.org/10.1017/ice.2016.179  PMID: 27523304 

Data & Media loading...

Supplementary data

Submit comment
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error