European Journal of Pediatrics

, Volume 174, Issue 6, pp 783–790 | Cite as

Pathogens causing urinary tract infections in infants: a European overview by the ESCAPE study group

  • Irene Alberici
  • Aysun Karabay Bayazit
  • Dorota Drozdz
  • Sevinç Emre
  • Michel Fischbach
  • Jérôme Harambat
  • Augustina Jankauskiene
  • Mieczyslaw Litwin
  • Sevgi Mir
  • William Morello
  • Amira Peco-Antic
  • Peter Sallay
  • Lale Sever
  • Giacomo D. Simonetti
  • Przemyslaw Szczesniak
  • Ana Teixeira
  • Enrico Vidal
  • Elke Wuehl
  • Otto Mehls
  • Lutz T. Weber
  • Franz Schaefer
  • Giovanni MontiniEmail author
  • for the ESCAPE study group and the PREDICT trial
Original Article


Knowledge of the distribution spectrum of causative organisms and their resistance patterns has become a core requirement for the rational and effective management of urinary tract infections. In the context of a prospective trial on the use of antibiotic prophylaxis in infants with underling kidney malformations, we conducted an online survey among paediatric nephrologists on positive urine cultures (July 2010–June 2012) from both hospitalized and non-hospitalized infants under 24 months of age. We collected 4745 urine cultures (UCs) at 18 units in 10 European countries. Escherichia coli was the most frequent bacterium isolated from UCs; however, in 10/16 hospitals and in 6/15 community settings, E. coli was isolated in less than 50 % of the total positive UCs. Other bacterial strains were Klebsiella, Enterococcus, Proteus and Pseudomonas not only from hospital settings. E. coli showed a high resistance to amoxicillin and trimethoprim and variable to cephalosporin. Nitrofurantoin had a good rate of efficacy, with 11/16 hospitals and 11/14 community settings reporting a resistance lower than 5 %.

Conclusion: E. coli is the most common organism causing UTIs in infants; however, other bacterial strains are frequently isolated. As a result, antibiotic prophylaxis should be more elastic and adaptable over time in order to guarantee maximum efficacy.


Urinary tract infection Antibiotic resistance Infants Escherichia coli Urine culture 



Clinical and Laboratory Standards Institute


European Committee for Antimicrobial Susceptibility Testing


Urine cultures


Urinary tract infection


Vesico-ureteral reflux



Thanks to all the microbiology departments for the support given to the authors in the selection of the data: Simone Ambretti (Bologna), Akgun Yaman (Adana), Joanna Klepacka (Krakow), Derya Aydin (Istanbul), Jaulhac Benoit (Strasbourg), Emilie Bessede (Bordeaux), Genovaite Bernatoniene (Vilnius), Suzana Laban-Nestorović (Belgrade), Eva Kenesei (Budapest), Nigar Çelik Özer (Istanbul), SC Droz (Bern), Anna Komarnicka (Gdansk), Lucia Rossi (Padova), Irene Burckhardt (Heidelberg) and Johannes Huebner (Munich).


  1. 1.
    Academy of Pediatrics subcommittee on Urinary Tract Infection, Steering Committee on Quality Improvement and Management (2011) Urinary Tract Infection: clinical practice guideline for the diagnosis and management of the initial UTI in febrile infants and children 2 to 24 months. Pediatrics 128:595CrossRefGoogle Scholar
  2. 2.
    Ammenti A, Cataldi L, Chimenz R, Fanos V, La Manna A, Marra G, Materassi M, Pecile P, Pennesi M, Pisanello L, Sica F, Toffolo A, Montini G, Italian Society of Pediatric Nephrology (2012) Febrile urinary tract infection in young children. Recommendations for the diagnosis, treatment and follow-up. Acta Paediatr 101(5):451–457CrossRefPubMedGoogle Scholar
  3. 3.
    Ashkenazi S (2012) Beginning and possibility the end of the antibiotic era. J Paediatr Child Health 49:E179–E182CrossRefPubMedGoogle Scholar
  4. 4.
    Beetz R, Westenfelder M (2011) Antimicrobial therapy of urinary tract infections in children. Int J Antimicrob Agents 38:42–50CrossRefPubMedGoogle Scholar
  5. 5.
    Bertrand X, Dowzick MJ (2012) Antimicrobial susceptibility among gram-negative isolates collected from intensive care units in north America, Europe, the Asia-pacific rim, Latin America, the Middle East, and Africa between 2004 and 2009 as part of the tigecycline evaluation and surveillance trial. Clin Ther 34(1):124–137CrossRefPubMedGoogle Scholar
  6. 6.
    Boggan J, Navar-Boggan A, Jhaveri R (2012) Pediatric-specific antimicrobial susceptibility data and empiric antibiotic selection. Pediatrics 130:e615–e622CrossRefPubMedGoogle Scholar
  7. 7.
    Catal F, Bavbek N, Bayrak O, Karabel M, Karabel D, Odemis E, Uz E (2009) Antimicrobial resistance patterns of urinary tract pathogens and rationale for empirical therapy in Turkish children for the years 2000–2006. Int Urol Nephrol 41:953–957CrossRefPubMedGoogle Scholar
  8. 8.
    CDC Antibiotic resistance threats in the United States 2013[ ]
  9. 9.
    Chavez-Bueno S, Stull TL (2009) Antibacterial agents in pediatrics. Infect Dis Clin N Am 23:865–880CrossRefGoogle Scholar
  10. 10.
    Cheng C, Tsai MH, Huang YC, Su LH, Tsau YK, Lin CJ, Chiu CH, Lin TY (2008) antibiotic resistance patterns of community-acquired urinary tract infections in children with vesicoureteral reflux receiving prophylactic antibiotic therapy. Pediatrics 122:1212–1217CrossRefPubMedGoogle Scholar
  11. 11. Identifier: NCT02021006Google Scholar
  12. 12.
    Coraggio MJ, Gross TP, Roscelli JD (1989) Nitrofurantoin toxicity in children. J Pediatr Infect Dis 8:163–168Google Scholar
  13. 13.
    Cullen IM, Manecksha RP, McCullagh E, Ahmad S, O’Kelly F, Flynn R, McDermott TE, Murphy P, Grainger R, Fennell JP, Thornhill JA (2013) An 11-year analysis of the prevalent uropathogens and the changing pattern of Escherichia coli antibiotic resistance in 38,530 community urinary tract infections, Dubllin 1999–2009. Ir J Med Sci 182:81–89CrossRefPubMedGoogle Scholar
  14. 14.
    David MZ, Crawford SE, Boyle-Vavra S, Hostetler AM, Kim DC, Daum RS (2006) Contrasting pediatric and adult methicillin-resistant Staphylococcus aureus isolates. Emerg Infect Dis 12(4):631–637CrossRefPubMedCentralPubMedGoogle Scholar
  15. 15.
  16. 16.
    Elliott SP (2008) Antimicrobial-resistant pathogens: an emerging pediatric threat. Adv Pediatr 55(1):329–348CrossRefPubMedGoogle Scholar
  17. 17.
    Gaspari R, Dickson E, Karlowsky J, Doern G (2005) Antibiotic resistance trends in paediatric uropathogens. Int J Antimicrob Agents 26:267–271CrossRefPubMedGoogle Scholar
  18. 18.
    Goossen H, Ferech M, Stichele RV, Elseviers M, for the ESAC Project Group (2005) Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet 365:379–387CrossRefGoogle Scholar
  19. 19.
    Hellerstein S (1982) Recurrent urinary tract infection in children. Pediatr Infect Dis J 1:271–281CrossRefGoogle Scholar
  20. 20.
    Hellström A, Hanson E, Hansson S, Hjälmås K, Jodal U (1991) Association between urinary symptoms at 7 years old and previous urinary tract infection. Arch Dis Child 66(2):232–234CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Holmberg L, Boman G, Böttiger LE, Eriksson B, Spross R, Wessling A (1980) Adverse reactions to nitrofurantoin. Analysis of 921 reports. Am I Med 69:733–738CrossRefGoogle Scholar
  22. 22.
    Hyun D, Hersh A, Namtu K, Palazzi D, Maples H, Newland J, Saiman L (2013) Antimicrobial stewardship in pediatrics: How every pediatrician can be a steward. JAMA Pediatr 167(9):859–866CrossRefPubMedGoogle Scholar
  23. 23.
    Karlowsky J, Karlowsky JA, Lagacé-Wiens PRS, Simner PJ, DeCorby MR, Adam HJ, Walkty A, Hoban DJ, Zhanel GG (2011) Antimicrobial resistance in urinary tract pathogens in Canada from 2007 to 2009: CANWARD Surveillance Study. Antimicrob Agents Chemotherapy 55:3169–3175CrossRefGoogle Scholar
  24. 24.
    Ladhani S, Gransden W (2003) Increasing antibiotic resistance among urinary tract isolates. Arch Dis Child 88:444–445CrossRefPubMedCentralPubMedGoogle Scholar
  25. 25.
    Marcus N, Ashkenazi S, Yaari A, Samra Z, Livni G (2005) Non-Escherichia coli versus Escherichia coli community-acquired urinary tract infections in children hospitalized in a tertiary center. Pediatr Infect Dis J 24:581–585CrossRefPubMedGoogle Scholar
  26. 26.
    Montini G, Rigon L, Zucchetta P, Fregonese F, Toffolo A, Gobber D, Cecchin D, Pavanello L, Molinari PP, Maschio F, Zanchetta S, Cassar W, Casadio L, Crivellaro C, Fortunati P, Corsini A, Calderan A, Comacchio S, Tommasi L, Hewitt IK, Da Dalt L, Zaccheelo G, Dall’Amico R, IRIS Group (2008) Prophylaxis after first febrile urinary tract infection in children? A multicenter, randomized, controlled, non inferiority trial. Pediatrics 122(5):1064–1071CrossRefPubMedGoogle Scholar
  27. 27.
    National Institute for Health and Clinical Excellence. Urinary tract infection in children: diagnosis, treatment and long term management. August 2007. []
  28. 28.
    Newman TB, Bernzweig JA, Takayama JI, Finch SA, Wasserman RC, Pantell RH (2002) Urine testing and urinary tract infections in febrile infants seen in office settings: the Pediatric Research in Office Settings’ Febrile Infant Study. Arch Pediatr Adolesc Med 156:44–54CrossRefPubMedGoogle Scholar
  29. 29.
    O’Brien TF (2011) What has kept the antibiotic miracle alive? N Engl J Med 365:953–955CrossRefPubMedGoogle Scholar
  30. 30.
    Peco-Antic A, Paripovic D, Buljugic S, Kruscic D, Spasojevic B, Cvetkovic M, Kostic M, Laban-Nestorovic S, Milosevski-Lomic G (2012) Antibiotic resistance of uropathogens in newborn and young children with acute pyelonephritis. Srp Arh Celok Lek 140:179–183CrossRefPubMedGoogle Scholar
  31. 31.
    Peters CA, Skoog SJ, Arant BS Jr, Coppo HL, Elder JS, Hudson RG, Khoury AE, Lorenzo AJ, Pohl HG, Shapiro E, Snodgrass WT, Diaz M (2010) Summary of the AUA Guidelines on management of primary vesicoureteral reflux in children. J Urol 184:1134–1144CrossRefPubMedGoogle Scholar
  32. 32.
    Smith SP, Manges AR, Riley LW (2008) Temporal changes in the prevalence of community-acquired antimicrobial-resistant urinary tract infection affected by Escherichia coli clonal group composition. Clin Infect Dis 46(5):689–695CrossRefPubMedGoogle Scholar
  33. 33.
    Tekgül S, Riedmiller H, Hoebeke P, Kocvara R, Nijman RJ, Radmayr C, Stein R, Dogan HS, European Association of Urology (2012) EAU Guidelines on vesicoureteral reflux in children. Eur Urol 62:534–542CrossRefPubMedGoogle Scholar
  34. 34.
    The ESCAPE Trial Group (2009) Strict blood-pressure control and progression of renal failure in children. N Engl J Med 361:1639–1650CrossRefGoogle Scholar
  35. 35.
    Tonkic M, Barisk IG, Punda-Polic V (2005) Prevalence and antimicrobial resistance of extended-spectrum beta-lactamases-producing Escherichia coli and Klebsiella pneumoniae strains isolated in a university hospital in Split, Croatia. Int Microbiol 8(2):119–124PubMedGoogle Scholar
  36. 36.
    Versporten A, Sharland M, Bielicki J, Drapier N, Vankerckhoven V, Goossens H (2012) The antibiotic resistance and prescribing in European Children project: a neonatal and pediatric antimicrobial web-based point prevalence survey in 73 hospitals worldwide. Pediatr Infect Dis J 32:e242–e253CrossRefGoogle Scholar
  37. 37.
    Yuksel S, Oztürk B, Kavaz A, Ozçakar ZB, Acar B, Güriz H, Aysev D, Ekim M, Yalçinkaya F (2006) Antibiotic resistance of urinary tract pathogens and evaluation of empirical treatment in Turkish children with urinary tract infectious. Int J Antimicrob Agents 28:413–416CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Irene Alberici
    • 1
  • Aysun Karabay Bayazit
    • 2
  • Dorota Drozdz
    • 3
  • Sevinç Emre
    • 4
  • Michel Fischbach
    • 5
  • Jérôme Harambat
    • 6
  • Augustina Jankauskiene
    • 7
  • Mieczyslaw Litwin
    • 8
  • Sevgi Mir
    • 9
  • William Morello
    • 1
  • Amira Peco-Antic
    • 10
  • Peter Sallay
    • 11
  • Lale Sever
    • 12
  • Giacomo D. Simonetti
    • 13
  • Przemyslaw Szczesniak
    • 14
  • Ana Teixeira
    • 15
  • Enrico Vidal
    • 16
  • Elke Wuehl
    • 17
  • Otto Mehls
    • 17
  • Lutz T. Weber
    • 18
  • Franz Schaefer
    • 17
  • Giovanni Montini
    • 1
    Email author
  • for the ESCAPE study group and the PREDICT trial
  1. 1.Nephrology and Dialysis Unit, Department of PediatricsAzienda Ospedaliera Universitaria Sant’Orsola-Malpighi BolognaBolognaItaly
  2. 2.Division of Pediatric Nephrology, School of MedicineCukurova UniversityAdanaTurkey
  3. 3.Dialysis UnitJagielloniam UniversityKrakowPoland
  4. 4.Pediatric Nephrology Department, Istanbul Medical FacultyIstanbul UniversityIstanbulTurkey
  5. 5.Service de PédiatrieCentre Hospitalier Universitaire HautepierreStrasbourgFrance
  6. 6.Service de Pédiatrie, Centre de Reference Maladies Rénales Rares du Sud OuestCentre Hospitalier Universitaire de BordeauxBordeauxFrance
  7. 7.Vilnius University Children HospitalVilniusLithuania
  8. 8.Department of NephrologyThe Children’s Memorial Health InstituteWarsawPoland
  9. 9.Faculty of MedicineEge UniversityIzmirTurkey
  10. 10.Division of Pediatric NephrologyUniversity Children’s HospitalBelgradeSerbia
  11. 11.Department of PediatricsSemmelweis UniversityBudapestHungary
  12. 12.Cerrahpasa School of MedicineIstanbul UniversityIstanbulTurkey
  13. 13.Pediatric NephrologyUniversity Children’s HospitalBernSwitzerland
  14. 14.Department Paediatrics, Nephrology and HypertensionMedical University GdanskGdanskPoland
  15. 15.Pediatric NephrologyUniversity Children’s HospitalPortoPortugal
  16. 16.Pediatric Nephrology, Dialysis and Transplantation Unit, Department of PediatricsUniversity of PadovaPadovaItaly
  17. 17.Division of Pediatric Nephrology, Center for Pediatrics and Adolescent MedicineUniversity of HeidelbergHeidelbergGermany
  18. 18.Pediatric Nephrology, Children’s and Adolescent’s HospitalUniversity Hospital of CologneCologneGermany

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