Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 25, Number 4—April 2019

Pneumonia-Specific Escherichia coli with Distinct Phylogenetic and Virulence Profiles, France, 2012–2014

Béatrice La Combe, Olivier Clermont, Jonathan Messika, Matthieu Eveillard, Achille Kouatchet, Sigismond Lasocki, Stéphane Corvec, Karim Lakhal, Typhaine Billard-Pomares, Romain Fernandes, Laurence Armand-Lefevre, Sandra Bourdon, Jean Reignier, Vincent Fihman, Nicolas de Prost, Julien Bador, Julien Goret, Frederic Wallet, Erick Denamur, Jean-Damien RicardComments to Author , on behalf of the COLOCOLI group
Author affiliations: Infection, Antimicrobiens, Modélisation, Évolution, Paris, France (B. La Combe, O. Clermont, J. Messika, T. Billard-Pomares, R. Fernandes, L. Armand-Lefevre, E. Denamur, J.-D. Ricard); Université Paris Diderot, Paris (B. La Combe, O. Clermont, J. Messika, T. Billard-Pomares, R. Fernandes, L. Armand-Lefevre, E. Denamur, J.-D. Ricard); Hôpital Louis Mourier, Colombes, France (B. La Combe, J. Messika, T. Billard-Pomares, R. Fernandes, J.-D. Ricard); Centre Hospitalier Universitaire, Angers, France (M. Eveillard, A. Kouatchet, S. Lasocki); Centre Hospitalier Universitaire, Nantes, France (S. Corvec, J. Reignier); Hôpital Laënnec, Nantes (K. Lakhal); Hôpital Bichat, AP-HP, Paris (L. Armand-Lefevre, E. Denamur); Centre Hospitalier Départemental Vendée, La Roche-sur-Yon, France (S. Bourdon); Hôpital Henri Mondor, AP-HP, Créteil, France (V. Fihman, N. de Prost); Centre Hospitalier Universitaire Bocage Central, Dijon, France (J. Bador); Centre Hospitalier Universitaire Pellegrin, Bordeaux, France (J. Goret); Centre Hospitalier Régional Universitaire, Lille, France (F. Wallet)

Main Article


Comparison of Escherichia coli isolates among pneumonia patients with extraintestinal infections, France, 2012–2014, with commensal E. coli (COLIVILLE collection) and E. coli bacteremia isolates (COLIBAFI collection). A) Proportions of E. coli phylogenetic groups and subgroups; B) B2 subgroups, D CGA, and B1 CC87; C) virulence factors; and D) antimicrobial drug resistance. Roman numerals correspond to the B2 subgroup. Correspondence with the Achtman multilocus sequence typing schema is as follow

Figure. Comparison of Escherichia coli isolates among pneumonia patients with extraintestinal infections, France, 2012–2014, with commensal E. coli (COLIVILLE collection) and E. coli bacteremia isolates (COLIBAFI collection). A) Proportions of E. coli phylogenetic groups and subgroups; B) B2 subgroups, D CGA, and B1 CC87; C) virulence factors; and D) antimicrobial drug resistance. Roman numerals correspond to the B2 subgroup. Correspondence with the Achtman multilocus sequence typing schema is as follows: subgroup I, STc131; subgroup II, STc73; subgroup III, STc127; subgroup IV, STc141; subgroup VI, STc12; subgroup VII, STc14; subgroup IX, STc95 (22). Proportions of subgroups are reported as fractions of the respective phylogroups. Asterisks indicate a significant difference between respiratory isolates and strains responsible for bacteremia (COLIBAFI collection) or commensal strains (COLIVILLE collection): *p<0.05; **p<0.005; ***p<0.0005. AMC, amoxicillin/clavulanic acid; AMK, amikacin; AMX, amoxicillin; CTX, cefotaxime; FOX, cefoxitin; OFX, ofloxacin; STc, sequence type complex.

Main Article

  1. Melsen  WG, Rovers  MM, Groenwold  RHH, Bergmans  DCJJ, Camus  C, Bauer  TT, et al. Attributable mortality of ventilator-associated pneumonia: a meta-analysis of individual patient data from randomised prevention studies. Lancet Infect Dis. 2013;13:66571. DOIPubMedGoogle Scholar
  2. Chastre  J, Fagon  J-Y. Ventilator-associated pneumonia. Am J Respir Crit Care Med. 2002;165:867903. DOIPubMedGoogle Scholar
  3. Russo  TA, Johnson  JR. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect. 2003;5:44956. DOIPubMedGoogle Scholar
  4. Kollef  MH, Ricard  J-D, Roux  D, Francois  B, Ischaki  E, Rozgonyi  Z, et al. A randomized trial of the amikacin fosfomycin inhalation system for the adjunctive therapy of gram-negative ventilator-associated pneumonia: IASIS Trial. Chest. 2017;151:123946. DOIPubMedGoogle Scholar
  5. Fihman  V, Messika  J, Hajage  D, Tournier  V, Gaudry  S, Magdoud  F, et al. Five-year trends for ventilator-associated pneumonia: Correlation between microbiological findings and antimicrobial drug consumption. Int J Antimicrob Agents. 2015;46:51825. DOIPubMedGoogle Scholar
  6. Hamet  M, Pavon  A, Dalle  F, Pechinot  A, Prin  S, Quenot  J-P, et al. Candida spp. airway colonization could promote antibiotic-resistant bacteria selection in patients with suspected ventilator-associated pneumonia. Intensive Care Med. 2012;38:12729. DOIPubMedGoogle Scholar
  7. World Health Organization. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics [cited 2017 Sep 29].
  8. Johnson  JR, Russo  TA. Extraintestinal pathogenic Escherichia coli: “the other bad E coli”. J Lab Clin Med. 2002;139:15562. DOIPubMedGoogle Scholar
  9. Johnson  JR, Kuskowski  MA, Gajewski  A, Soto  S, Horcajada  JP, Jimenez de Anta  MT, et al. Extended virulence genotypes and phylogenetic background of Escherichia coli isolates from patients with cystitis, pyelonephritis, or prostatitis. J Infect Dis. 2005;191:4650. DOIPubMedGoogle Scholar
  10. Johnson  JR, Kuskowski  MA, O’Bryan  TT, Maslow  JN. Epidemiological correlates of virulence genotype and phylogenetic background among Escherichia coli blood isolates from adults with diverse-source bacteremia. J Infect Dis. 2002;185:143947. DOIPubMedGoogle Scholar
  11. Lefort  A, Panhard  X, Clermont  O, Woerther  P-L, Branger  C, Mentré  F, et al.; COLIBAFI Group. Host factors and portal of entry outweigh bacterial determinants to predict the severity of Escherichia coli bacteremia. J Clin Microbiol. 2011;49:77783. DOIPubMedGoogle Scholar
  12. Bidet  P, Mahjoub-Messai  F, Blanco  J, Blanco  J, Dehem  M, Aujard  Y, et al. Combined multilocus sequence typing and O serogrouping distinguishes Escherichia coli subtypes associated with infant urosepsis and/or meningitis. J Infect Dis. 2007;196:297303. DOIPubMedGoogle Scholar
  13. Bingen  E, Picard  B, Brahimi  N, Mathy  S, Desjardins  P, Elion  J, et al. Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J Infect Dis. 1998;177:64250. DOIPubMedGoogle Scholar
  14. Bert  F, Johnson  JR, Ouattara  B, Leflon-Guibout  V, Johnston  B, Marcon  E, et al. Genetic diversity and virulence profiles of Escherichia coli isolates causing spontaneous bacterial peritonitis and bacteremia in patients with cirrhosis. J Clin Microbiol. 2010;48:270914. DOIPubMedGoogle Scholar
  15. Messika  J, Magdoud  F, Clermont  O, Margetis  D, Gaudry  S, Roux  D, et al. Pathophysiology of Escherichia coli ventilator-associated pneumonia: implication of highly virulent extraintestinal pathogenic strains. Intensive Care Med. 2012;38:200716. DOIPubMedGoogle Scholar
  16. Blanco  J, Mora  A, Mamani  R, López  C, Blanco  M, Dahbi  G, et al. National survey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal groups O25b:H4-B2-ST131, O15:H1-D-ST393 and CGA-D-ST69 with high virulence gene content in Spain. J Antimicrob Chemother. 2011;66:201121. DOIPubMedGoogle Scholar
  17. American Thoracic SocietyInfectious Diseases Society of America. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med. 2005;171:388416. DOIPubMedGoogle Scholar
  18. Clermont  O, Christenson  JK, Denamur  E, Gordon  DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep. 2013;5:5865. DOIPubMedGoogle Scholar
  19. Skurnik  D, Clermont  O, Guillard  T, Launay  A, Danilchanka  O, Pons  S, et al. Emergence of antimicrobial-resistant Escherichia coli of animal origin spreading in humans. Mol Biol Evol. 2016;33:898914. DOIPubMedGoogle Scholar
  20. Clermont  O, Christenson  JK, Daubié  A-S, Gordon  DM, Denamur  E. Development of an allele-specific PCR for Escherichia coli B2 sub-typing, a rapid and easy to perform substitute of multilocus sequence typing. J Microbiol Methods. 2014;101:247. DOIPubMedGoogle Scholar
  21. Johnson  JR, Owens  K, Manges  AR, Riley  LW. Rapid and specific detection of Escherichia coli clonal group A by gene-specific PCR. J Clin Microbiol. 2004;42:261822. DOIPubMedGoogle Scholar
  22. Clermont  O, Gordon  D, Denamur  E. Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiology. 2015;161:9808. DOIPubMedGoogle Scholar
  23. Clermont  O, Johnson  JR, Menard  M, Denamur  E. Determination of Escherichia coli O types by allele-specific polymerase chain reaction: application to the O types involved in human septicemia. Diagn Microbiol Infect Dis. 2007;57:12936. DOIPubMedGoogle Scholar
  24. Eckert  C, Gautier  V, Saladin-Allard  M, Hidri  N, Verdet  C, Ould-Hocine  Z, et al. Dissemination of CTX-M-type beta-lactamases among clinical isolates of Enterobacteriaceae in Paris, France. Antimicrob Agents Chemother. 2004;48:124955. DOIPubMedGoogle Scholar
  25. Rasheed  JK, Jay  C, Metchock  B, Berkowitz  F, Weigel  L, Crellin  J, et al. Evolution of extended-spectrum beta-lactam resistance (SHV-8) in a strain of Escherichia coli during multiple episodes of bacteremia. Antimicrob Agents Chemother. 1997;41:64753. DOIPubMedGoogle Scholar
  26. Massot  M, Daubié  A-S, Clermont  O, Jauréguy  F, Couffignal  C, Dahbi  G, et al.; The Coliville Group. Phylogenetic, virulence and antibiotic resistance characteristics of commensal strain populations of Escherichia coli from community subjects in the Paris area in 2010 and evolution over 30 years. Microbiology. 2016;162:64250. DOIPubMedGoogle Scholar
  27. Clermont  O, Couffignal  C, Blanco  J, Mentré  F, Picard  B, Denamur  E; COLIVILLE and COLIBAFI groups. Two levels of specialization in bacteraemic Escherichia coli strains revealed by their comparison with commensal strains. Epidemiol Infect. 2017;145:87282. DOIPubMedGoogle Scholar
  28. Bender  R, Lange  S. Adjusting for multiple testing—when and how? J Clin Epidemiol. 2001;54:3439. DOIPubMedGoogle Scholar
  29. Johnson  JR, Menard  ME, Lauderdale  T-L, Kosmidis  C, Gordon  D, Collignon  P, et al.; Trans-Global Initiative for Antimicrobial Resistance Analysis Investigators. Global distribution and epidemiologic associations of Escherichia coli clonal group A, 1998-2007. Emerg Infect Dis. 2011;17:20019. DOIPubMedGoogle Scholar
  30. Brzuszkiewicz  E, Brüggemann  H, Liesegang  H, Emmerth  M, Olschläger  T, Nagy  G, et al. How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci U S A. 2006;103:1287984. DOIPubMedGoogle Scholar
  31. Croxen  MA, Finlay  BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol. 2010;8:2638. DOIPubMedGoogle Scholar
  32. Russo  TA, Johnson  JR. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis. 2000;181:17534. DOIPubMedGoogle Scholar
  33. Dale  AP, Woodford  N. Extra-intestinal pathogenic Escherichia coli (ExPEC): Disease, carriage and clones. J Infect. 2015;71:61526. DOIPubMedGoogle Scholar
  34. Picard  B, Garcia  JS, Gouriou  S, Duriez  P, Brahimi  N, Bingen  E, et al. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun. 1999;67:54653.PubMedGoogle Scholar
  35. Ciesielczuk  H, Jenkins  C, Chattaway  M, Doumith  M, Hope  R, Woodford  N, et al. Trends in ExPEC serogroups in the UK and their significance. Eur J Clin Microbiol Infect Dis. 2016;35:16616. DOIPubMedGoogle Scholar
  36. Kallonen  T, Brodrick  HJ, Harris  SR, Corander  J, Brown  NM, Martin  V, et al. Systematic longitudinal survey of invasive Escherichia coli in England demonstrates a stable population structure only transiently disturbed by the emergence of ST131. Genome Res. 2017;27:143749. DOIPubMedGoogle Scholar
  37. Phillips-Houlbracq  M, Ricard  J-D, Foucrier  A, Yoder-Himes  D, Gaudry  S, Bex  J, et al. Pathophysiology of Escherichia coli pneumonia: Respective contribution of pathogenicity islands to virulence. Int J Med Microbiol. 2018;308:2906. DOIPubMedGoogle Scholar
  38. Tourret  J, Diard  M, Garry  L, Matic  I, Denamur  E. Effects of single and multiple pathogenicity island deletions on uropathogenic Escherichia coli strain 536 intrinsic extra-intestinal virulence. Int J Med Microbiol. 2010;300:4359. DOIPubMedGoogle Scholar
  39. Russo  TA, Davidson  BA, Genagon  SA, Warholic  NM, Macdonald  U, Pawlicki  PD, et al. E. coli virulence factor hemolysin induces neutrophil apoptosis and necrosis/lysis in vitro and necrosis/lysis and lung injury in a rat pneumonia model. Am J Physiol Lung Cell Mol Physiol. 2005;289:L20716. DOIPubMedGoogle Scholar
  40. Roux  D, Danilchanka  O, Guillard  T, Cattoir  V, Aschard  H, Fu  Y, et al. Fitness cost of antibiotic susceptibility during bacterial infection. Sci Transl Med. 2015;7:297ra114. DOIPubMedGoogle Scholar
  41. Garrouste-Orgeas  M, Chevret  S, Arlet  G, Marie  O, Rouveau  M, Popoff  N, et al. Oropharyngeal or gastric colonization and nosocomial pneumonia in adult intensive care unit patients. A prospective study based on genomic DNA analysis. Am J Respir Crit Care Med. 1997;156:164755. DOIPubMedGoogle Scholar
  42. Sabarly  V, Bouvet  O, Glodt  J, Clermont  O, Skurnik  D, Diancourt  L, et al. The decoupling between genetic structure and metabolic phenotypes in Escherichia coli leads to continuous phenotypic diversity. J Evol Biol. 2011;24:155971. DOIPubMedGoogle Scholar
  43. Bleibtreu  A, Gros  P-A, Laouénan  C, Clermont  O, Le Nagard  H, Picard  B, et al. Fitness, stress resistance, and extraintestinal virulence in Escherichia coli. Infect Immun. 2013;81:273342. DOIPubMedGoogle Scholar

Main Article

1Group members are listed at the end of this article.

Page created: March 04, 2019
Page updated: March 04, 2019
Page reviewed: March 04, 2019
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.