Skip to main content

Advertisement

Log in

Commonality of adherent-invasive Escherichia coli isolated from patients with extraintestinal infections, healthy individuals and the environment

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Adherent-invasive Escherichia coli (AIEC) has been implicated as a microbiological factor in inflammatory bowel disease (IBD) pathogenesis. These strains are defined by their ability to adhere to and invade intestinal epithelial cells, and to survive and replicate in macrophages. We postulated that AIEC strains may commonly inhabit the gut of healthy individuals (HI), cause extraintestinal infections, and be found in sewage treatment plants (STP) and surface waters (SW). A total of 808 E. coli strains isolated from HI; patients with community-acquired urinary tract infection (CA-UTI), septicaemia and urosepsis; STP; and SW, showing a diffuse adhesion pattern to Caco-2 cells were included in this study. Typing of the strains using a combination of RAPD-PCR and PhPlate fingerprinting grouped them into 48 common clones (CCs). Representatives of each CC were tested for the ability to invade Caco-2 cells, survive and replicate in macrophages, and for the presence of six virulence genes commonly found among AIEC strains. Twenty CCs were deemed AIEC based on their ability to survive and replicate in macrophages, while encoding htrA, dsbA and clbA genes. These CCs primarily originated from HI and CA-UTI patients but were also detected in secondary locations including STP and SW. Strains lacking intramacrophagic survival and replication abilities were regarded as diffusely adhering E. coli (DAEC). Certain clones of AIEC are common in the gut of HI whilst promoting CA-UTI. The survival and persistence of AIEC in STP and SW may have serious public health ramifications for individuals predisposed to IBD.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Zhang Y-Z, Li Y-Y (2014) Inflammatory bowel disease: pathogenesis. World J Gastroenterol 20(1):91–99. https://doi.org/10.3748/wjg.v20.i1.91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Flanagan P, Campbell BJ, Rhodes JM (2011) Bacteria in the pathogenesis of inflammatory bowel disease. Biochem Soc Trans 39(4):1067–1072. https://doi.org/10.1042/BST0391067

    Article  CAS  PubMed  Google Scholar 

  3. Burisch J, Jess T, Martinato M, Lakatos PL (2013) The burden of inflammatory bowel disease in Europe. J Crohns Colitis 7(4):322–337. https://doi.org/10.1016/j.crohns.2013.01.010

    Article  PubMed  Google Scholar 

  4. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB (2013) Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26(4):822–880. https://doi.org/10.1128/CMR.00022-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chassaing B, Rolhion N, de Vallée A, Sa’ad YS, Prorok-Hamon M, Neut C, Campbell BJ, Söderholm JD, Hugot J-P, Colombel J-F (2011) Crohn disease–associated adherent-invasive E. coli bacteria target mouse and human Peyer’s patches via long polar fimbriae. J Clin Invest 121(3):966–975. https://doi.org/10.1172/JCI44632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Willing B, Halfvarson J, Dicksved J, Rosenquist M, Järnerot G, Engstrand L, Tysk C, Jansson JK (2009) Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn’s disease. Inflamm Bowel Dis 15(5):653–660. https://doi.org/10.1002/ibd.20783

    Article  PubMed  Google Scholar 

  7. Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, Desreumaux P, Gambiez L, Joly B, Cortot A, Colombel J-F (1998) Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn’s disease. Gastroenterol 115(6):1405–1413. https://doi.org/10.1016/s0016-5085(98)70019-8

    Article  CAS  Google Scholar 

  8. Martinez-Medina M, Aldeguer X, Gonzalez-Huix F, Acero D, Garcia-Gil LJ (2006) Abnormal microbiota composition in the ileocolonic mucosa of Crohn's disease patients as revealed by polymerase chain reaction-denaturing gradient gel electrophoresis. Inflamm Bowel Dis 12(12):1136–1145. https://doi.org/10.1097/01.mib.0000235828.09305.0c

    Article  PubMed  Google Scholar 

  9. Martinez-Medina M, Aldeguer X, Lopez-Siles M, González-Huix F, López-Oliu C, Dahbi G, Blanco JE, Blanco J, Garcia-Gil LJ, Darfeuille-Michaud A (2009) Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn’s disease. Inflamm Bowel Dis 15(6):872–882. https://doi.org/10.1002/ibd.20860

    Article  PubMed  Google Scholar 

  10. Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM (2004) Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterol 127(1):80–93. https://doi.org/10.1053/j.gastro.2004.03.054

    Article  CAS  Google Scholar 

  11. Mylonaki M, Rayment NB, Rampton DS, Hudspith BN, Brostoff J (2005) Molecular characterisation of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm Bowel Dis 11(5):481–487. https://doi.org/10.1097/01.MIB.0000159663.62651.4f

    Article  PubMed  Google Scholar 

  12. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M (2002) Mucosal flora in inflammatory bowel disease. Gastroenterol 122(1):44–54. https://doi.org/10.1053/gast.2002.30294

    Article  Google Scholar 

  13. Swidsinski A, Khilkin M, Kerjaschki D, Schreiber S, Ortner M, Weber J, Lochs H (1998) Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterol 115(2):281–286. https://doi.org/10.1053/gast.2002.30294

    Article  CAS  Google Scholar 

  14. Kotlowski R, Bernstein CN, Sepehri S, Krause DO (2007) High prevalence of Escherichia coli belonging to the B2+ D phylogenetic group in inflammatory bowel disease. Gut 56(5):669–675. https://doi.org/10.1136/gut.2006.099796

    Article  CAS  PubMed  Google Scholar 

  15. Barnich N, Carvalho FA, Glasser A-L, Darcha C, Jantscheff P, Allez M, Peeters H, Bommelaer G, Desreumaux P, Colombel J-F (2007) CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonisation in Crohn disease. J Clin Invest 117(6):1566–1574. https://doi.org/10.1172/JCI30504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Carvalho FA, Barnich N, Sivignon A, Darcha C, Chan CHF, Stanners CP, Darfeuille-Michaud A (2009) Crohn’s disease adherent-invasive Escherichia coli colonise and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 206(10):2179–2189. https://doi.org/10.1084/jem.20090741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser A-L, Barnich N, Bringer M-A, Swidsinski A, Beaugerie L, Colombel J-F (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterol 127(2):412–421. https://doi.org/10.1053/j.gastro.2004.04.061

    Article  Google Scholar 

  18. Conte MP, Schippa S, Zamboni I, Penta M, Chiarini F, Seganti L, Osborn J, Falconieri P, Borrelli O, Cucchiara S (2006) Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut 55(12):1760–1767 https://doi.org/10.1136/gut.2005.078824

    Article  CAS  Google Scholar 

  19. Bringer M-A, Barnich N, Glasser A-L, Bardot O, Darfeuille-Michaud A (2005) HtrA stress protein is involved in intramacrophagic replication of adherent and invasive Escherichia coli strain LF82 isolated from a patient with Crohn’s disease. Infect Immun 73(2):712–721. https://doi.org/10.1128/IAI.73.2.712-721.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Glasser A-L, Boudeau J, Barnich N, Perruchot M-H, Colombel J-F, Darfeuille-Michaud A (2001) Adherent invasive Escherichia coli strains from patients with Crohn’s disease survive and replicate within macrophages without inducing host cell death. Infect Immun 69(9):5529–5537. https://doi.org/10.1128/iai.69.9.5529-5537.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Martinez-Medina M, Garcia-Gil LJ (2014) Escherichia coli in chronic inflammatory bowel diseases: an update on adherent invasive Escherichia coli pathogenicity. World J Gastrointest Pathophysiol 5(3):213–227. https://doi.org/10.4291/wjgp.v5.i3.213

    Article  PubMed  PubMed Central  Google Scholar 

  22. Dreux N, Denizot J, Martinez-Medina M, Mellman A, Billig M, Kisiela D, Chattopdhyay S, Sokurenko E, Neut C, Gower-Rousseau C (2013) Point mutations in FimH adhesin Crohn’s disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response. PLoS Pathog 9:e1003141

    Article  CAS  Google Scholar 

  23. Rolhion N, Barnich N, Bringer MA, Glasser AL, Ranc J, Hèbuterne X, Hofman P, Darfeuiile-Michaud A (2010) Abnormally expressed ER response chaperone Gp96 in CD favours adherent0invasive Escherichia coli invasion. Gastroenterol 59(10):1355–1362. https://doi.org/10.1136/gut.2010.207456

    Article  CAS  Google Scholar 

  24. Bringer M-A, Rolhion N, Glasser A-L, Darfeuille-Michaud A (2007) The oxidoreductase DsbA plays a key role in the ability of the Crohn’s disease-associated adherent-invasive Escherichia coli strain LF82 to resist macrophage killing. J Bacteriol 189(13):4860–4871. https://doi.org/10.1128/JB.00233-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan T-J, Campbell BJ, Abujamel T, Dogan B, Rogers AB (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338(6103):120–123. https://doi.org/10.1126/science.1224820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313(5788):848–851. https://doi.org/10.1126/science.1127059

    Article  CAS  PubMed  Google Scholar 

  27. Vollmerhausen TL, Ramos NL, Gündoğdu A, Robinson W, Brauner A, Katouli M (2011) Population structure and uropathogenic virulence-associated genes of faecal Escherichia coli from healthy young and elderly adults. J Med Microbiol 60(5):574–581. https://doi.org/10.1099/jmm.0.027037-0

    Article  PubMed  Google Scholar 

  28. Moreno E, Johnson JR, Pérez T, Prats G, Kuskowski MA, Andreu A (2009) Structure and urovirulence characteristics of the fecal Escherichia coli population among healthy women. Microbes Infect 11:274–280. https://doi.org/10.1016/j.micinf.2008.12.002

    Article  PubMed  Google Scholar 

  29. Nowrouzian FL, Wold AE, Adlerberth I (2005) Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J Infect Dis 191:1078–1083. https://doi.org/10.1111/j.1469-0691.2009.02706.x

    Article  CAS  PubMed  Google Scholar 

  30. Schlager TA, Hendley JO, Bell AL, Whittam TS (2002) Clonal diversity of Escherichia coli colonising stools and urinary tracts of young girls. Infect Immun 70:1225–1229. https://doi.org/10.1128/iai.70.3.1225-1229.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Schlager TA, Whittam TS, Hendley JO, Bhang JL, Wobbe CL, Stapleton A (2003) Variation in frequency of the virulence-factor gene in Escherichia coli clones colonising the stools and urinary tracts of healthy prepubertal girls. J Infect Dis 188:1059–1064. https://doi.org/10.1086/377643

    Article  PubMed  Google Scholar 

  32. Anastasi E, Matthews B, Stratton HM, Katouli M (2012) Pathogenic Escherichia coli found in sewage treatment plants and environmental waters. Appl Environ Microbiol 76:5882–5886. https://doi.org/10.1128/AEM.00141-10

    Article  CAS  Google Scholar 

  33. Anastasi EM, Matthews B, Gundogdu A, Vollmerhausen TL, Ramos NL, Stratton H, Ahmed W, Katouli M (2010) Prevalence and persistence of Escherichia coli strains with uropathogenic virulence characteristics in sewage treatment plants. Appl Environ Microbiol 78:5536–5541. https://doi.org/10.1128/AEM.00657-12

    Article  CAS  Google Scholar 

  34. Masters N, Wiegand A, Ahmed W, Katouli M (2011) Escherichia coli virulence genes profile of surface waters as an indicator of water quality. Water Res 45:6321. https://doi.org/10.1016/j.watres.2011.09.018

    Article  CAS  PubMed  Google Scholar 

  35. Ramos NL, Saayman ML, Chapman TA, Tucker JR, Smith HV, Faoagali J, Chin JC, Brauner A, Katouli M (2010) Genetic relatedness and virulence gene profiles of Escherichia coli strains isolated from septicaemic and uroseptic patients. Eur J Clin Microbiol Infect Dis 29:15–23. https://doi.org/10.1007/s10096-009-0809-2

    Article  CAS  PubMed  Google Scholar 

  36. Chen J, Griffiths MW (1998) PCR differentiation of Escherichia coli from other gram-negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein. Lett Appl Microbiol 27:369–371. https://doi.org/10.1046/j.1472-765x.1998.00445.x

    Article  CAS  PubMed  Google Scholar 

  37. Corney BG, Colley J, Djordjevic SP, Whittington R, Graham GC (1993) Rapid identification of some Leptospira isolates from cattle by random amplified polymorphic DNA fingerprinting. J Clin Microbiol 31(11):2927–2932. https://doi.org/10.1128/JCM.31.11.2927-2932.1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Nataro JP, Kaper JB, Robins-Browne R, Prado V, Vial P, Levine MM (1987) Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Paediatr Infect Dis J 6:829–831. https://doi.org/10.1097/00006454-198709000-00008

    Article  CAS  Google Scholar 

  39. Katouli M, Bark T, Ljungqvist O, Svenberg T, Möllby R (1994) Composition and diversity of intestinal coliform flora influence bacterial translocation in rats after hemorrhagic stress. Infect Immun 62(11):4768–477439. https://doi.org/10.1128/iai.62.11.4768-4774.1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Owrangi B, Masters N, Vollmerhausen T, O'Dea C, Kuballa A, Katouli M (2017) Comparison between virulence characteristics of dominant and non-dominant Escherichia coli strains of the gut and their interaction with Caco-2 cells. Microb Pathog 105:171–176. https://doi.org/10.1016/j.micpath.2017.02.032

    Article  CAS  PubMed  Google Scholar 

  41. Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylogroups. Environ Microbiol Rep 5(1):58–65. https://doi.org/10.1111/1758-2229.12019

    Article  CAS  PubMed  Google Scholar 

  42. Prorok-Hamon M, Friswell MK, Alswied A, Roberts CL, Song F, Flanagan PK, Knight P, Codling C, Marchesi JR, Winstanley C (2013) Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer. Gut:gutjnl-2013

  43. Martinez-Medina M, Garcia-Gil J, Barnich N, Wieler LH, Ewers C (2011) Adherent-invasive Escherichia coli phenotype displayed by intestinal pathogenic E. coli strains from cats, dogs, and swine. Appl Environ Microbiol 2011:5813–5817. https://doi.org/10.1128/AEM.0261410

    Article  Google Scholar 

  44. Goswami M, Khan FA, Ibrisevic A, Olsson PE, Jass J (2018) Development of Escherichia coli based gene expression profiling of sewage sludge leachates. J Appl Microbiol. https://doi.org/10.1111/jam.14028

  45. Servin AL (2014) Pathogenesis of human diffusely adhering Escherichia coli expressing Afa/Dr adhesins (Afa/Dr DAEC): current insights and future challenges. Clin Microbiol Rev 18:264–292. https://doi.org/10.1128/CMR.18.2.264-292.2005

    Article  CAS  Google Scholar 

  46. Gao Q, Wang X, Xu H, Xu Y, Ling J, Zhang D, Gao S, Liu X (2012) Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model. BMC Microbiol 12:143. https://doi.org/10.1186/1471-2180-12-143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Katouli.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study used collections of E. coli strains isolated from previous studies that had been stored at − 80 °C which did not require any ethical approval.

Informed consent

This is to certify that all authors named in this manuscript have read the contents of the manuscript and agree with its submission to the EJCMID.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Astley, D.J., Masters, N., Kuballa, A. et al. Commonality of adherent-invasive Escherichia coli isolated from patients with extraintestinal infections, healthy individuals and the environment. Eur J Clin Microbiol Infect Dis 40, 181–192 (2021). https://doi.org/10.1007/s10096-020-04066-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-020-04066-5

Keywords

Navigation