Abstract
Urinary tract infections (UTIs) are one of the most frequent infections in elderly people. The majority of infections is caused by uropathogenic E. coli. These strains contain a broad spectrum of virulence factors and are able to overcome defense barriers and colonize host organism. Population of elderly individuals has been growing globally and for that reason it is possible to expect a rise of UTIs among them. The aim of this study was to determine the phylogenetic group (A, B1, B2 and D) of urinary strains of E. coli isolated from elderly patients and evaluate the presence of 14 virulence genes (hly, cnf1, cdt, sat, afa, sfa, pap, aer, upaH, cah, pic, neuC, kpsMT II and traT) in these strains. We have carried out a phylogenetic analysis and virulence genes identification of 75 urinary E. coli isolates. Among our 75 E. coli strains, phylogenetic group B2 (64%) was the most dominant followed by groups D (16%), B1 (10.7%) and A (9.3%). The genes kpsMT II (65.3%), traT (61.3%), upaH (58.6%) and aer (52.0%) were found to be the most prevalent. We identified from 5 to 10 virulence genes in 44% strains belonging to B2 phylogroup. E. coli urinary strains examined in this study belonged mainly to phylogenetic group B2. We have also found that the majority of examined virulence genes, which are crucial for the establishment and maintenance of infection, were present in these strains.
Acknowledgements
This study was supported by the project VERZDRAV (ITMS: 26220220162).
Abbreviations
- UPEC
uropathogenic Escherichia coli
- UTI
urinary tract infection.
References
Abdi H.A. & Rashki A. 2014. Comparison of virulence factors distribution in uropathogenic E. coli isolates from phylogenetic groups B2 and D. Int. J. Enteric. Pathog. 2: e21725.10.17795/ijep21725Search in Google Scholar
Agarwal J., Mishra B., Srivastava S., Srivastava R. & Pandey A. 2014. Virulence determinants in Escherichia coli associated with recurrent cystitis in sexually active women. Microb. Pathog. 74: 38–41.10.1016/j.micpath.2014.07.004Search in Google Scholar PubMed
Allsopp L.P., Totsika M., Tree J.J., Ulett G.C., Mabbett A.N., Wells J.T., Kobe B., Beatson S.A. & Schembri M.A. 2010. upah is a newly identified autotransporter protein that contributes to biofilm formation and bladder colonization by uropathogenic Escherichia coli CFT073. Infect. Immun. 78: 1659–1669.10.1128/IAI.01010-09Search in Google Scholar PubMed PubMed Central
Bashir S., Haque A., Sarwar Y., Aamir A. & Anwar M. I. 2012. Virulence profile of different phylogenetic groups of locally isolated community acquired uropathogenic E. coli from Faisalabad region of Pakistan. Ann. Clin. Microbiol. Antimicrob. 11: 23.10.1186/1476-0711-11-23Search in Google Scholar PubMed PubMed Central
Biscola F.T., Abe M.C. & Guth B.E.C. 2011. Determination of adhesin gene sequences in, and biofilm formation by, O157 and non-O157 shiga toxin-producing Escherichia coli strains isolated from different sources. Appl. Environ. Microbiol. 77: 2201–2208.10.1128/AEM.01920-10Search in Google Scholar PubMed PubMed Central
Boisen N., Ruiz-Perez F., Scheutz F., Krogfelt K.A. & Nataro J. P. 2009. Short report: high prevalence of serine protease autotransporter cytotoxins among strains of enteroaggregative Escherichia coli. Am. J. Trop. Med. Hyg. 80: 294–301.10.4269/ajtmh.2009.80.294Search in Google Scholar
Clermont O., Bonacorsi S. & Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66: 4555–4558.10.1128/AEM.66.10.4555-4558.2000Search in Google Scholar PubMed PubMed Central
Čurová K., Kmeťová M. & Siegfried L. 2014. CDT toxíny. Epidemiol. Mikrobiol. Imunol. 63: 134–139.Search in Google Scholar
Dubois D., Delmas J., Cady A., Robin F., Sivignon A., Oswald E. & Bonnet R. 2010. Cyclomodulins in urosepsis strains of Escherichia coli. J. Clin. Microbiol. 48: 2122–2129.10.1128/JCM.02365-09Search in Google Scholar PubMed PubMed Central
Ejrnæs K. 2011. Bacterial characteristics of importance for recurrent urinary tract infections caused by Escherichia coli. Dan. Med. Bull. 58: B4187.Search in Google Scholar
Ejrnæs K., Stegger M., Reisner A., Ferry S., Monsen T., Holm S.E., Lundgren B. & Frimodt-Mřller N. 2011. Characteristic of Escherichia coli causing persistence or relapse of urinary tract infections: phylogenetic groups, virulence factors and biofilm formation. Virulence 2: 528–537.10.4161/viru.2.6.18189Search in Google Scholar PubMed
Farshad S. & Emamghorashi F. 2009. The prevalence of virulence genes of E. coli strains isolated from children with urinary tract infection. Saudi J. Kidney Dis. Transpl. 20: 613–617.Search in Google Scholar
Fattahi S., Kafil H.S., Nahai M.R., Asgharzadeh M., Nori R. & Aghazadeh M. 2015. Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS Hyg. Infect. Control. 10: 1–7.Search in Google Scholar
Ferreira D., Seca A.M.L., Pinto D.C.G.A. & Silva A.M.S. 2016. Targeting human pathogenic bacteria by siderophores: a proteomics review. J. Proteomics 145: 153–166.10.1016/j.jprot.2016.04.006Search in Google Scholar PubMed
Firoozeh F., Saffari M., Neamati F. & Zibaei M. 2014. Detection of virulence genes in Escherichia coli isolates from patients with cystitis and pyelonephritis. Int. J. Infect. Dis. 29: 219–222.10.1016/j.ijid.2014.03.1393Search in Google Scholar PubMed
Foxman B. 2010. The epidemiology of urinary tract infection. Nat. Rev. Urol. 7: 653–660.10.1038/nrurol.2010.190Search in Google Scholar PubMed
Garcia E.C., Brumbaugh A.R. & Mobley H.L.T. 2011. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect. Immun. 79: 1225–1235.10.1128/IAI.01222-10Search in Google Scholar PubMed PubMed Central
Guyer D.M., Gunther N.W. & Mobley H.L.T. 2001. Secreted proteins and other features specific to uropathogenic Escherichia coli. J. Infect. Dis. 183: 32–35.10.1086/318854Search in Google Scholar PubMed
Guyer D.M., Radulovic S., Jones F.E. & Mobley H.L.T. 2002. Sat, the secreted autotransporter toxin of uropathogenic Escherichia coli, is a vacuolating cytotoxin for bladder and kidney epithelial cells. Infect. Immun. 70: 4539–4546.10.1128/IAI.70.8.4539-4546.2002Search in Google Scholar PubMed PubMed Central
Heywood W., Henderson B. & Nair S.P. 2005. Cytolethal distending toxin: creating a gap in the cell cycle. J. Med. Microbiol. 54: 207–216.10.1099/jmm.0.45694-0Search in Google Scholar PubMed
Janka A., Bielaszewska M., Dobrindt U., Greune L., Schmidt M.A. & Karch H. 2003. cytolethal distending toxin gene cluster in enterohemorrhagic Escherichia coli O157:H- an O157:H7: characterization and evolutionary consideration. Infect. Immun. 71: 3634–3638.10.1128/IAI.71.6.3634-3638.2003Search in Google Scholar PubMed PubMed Central
Johnson J.R. 1991. Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev. 4: 80–128.10.1128/CMR.4.1.80Search in Google Scholar PubMed PubMed Central
Johnson J.R., Kuskowski M.A., Gajewski A., Soto S., Horcajada J.P., Jimeney de Anta M.T. & Vila J. 2005. Extended virulence genotypes and phylogenetic background of Escherichia coli isolates from patients with cystitis, pyelonephritis, or prostatitis. J. Infect. Dis. 191: 46–50.10.1086/426450Search in Google Scholar PubMed
Johnson J.R. & Stell A.L. 2000. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis. 181: 261–72.10.1086/315217Search in Google Scholar PubMed
Kadhum H.J., Finlay D., Rowe M.T., Wilson I.G. & Ball H.J. 2008. Occurrence and characteristics of cytotoxic necrotizing factors, cytolethal distending toxins and other virulence factors in Escherichia coli from human blood and faecal samples. Epidemiol. Infect. 136: 752–760.10.1017/S0950268807009247Search in Google Scholar PubMed PubMed Central
Karimian A., Momtaz H. & Madani M. 2012. Detection of uropathogenic Escherichia coli virulence factors in patients with urinary tract infections in Iran. Afr. J. Microbiol. Res. 6: 6811–6816.10.5897/AJMR12.1462Search in Google Scholar
Katouli M. 2010. Population structure of gut Escherichia coli and its role in development of extra-intestinal infections. Iran. J. Microbiol. 2: 59–72.Search in Google Scholar
Kline K.A. & Bowdish D.M.E. 2016. Infections in an aging population. Curr. Opin. Microbiol. 29: 63–67.10.1016/j.mib.2015.11.003Search in Google Scholar PubMed
Kmeťová M., Kendrovská E., Takáčová V., Sabol M. & Siegfried L. 2012. Virulentný profil a rezistencia Escherichia coli izolovaných od imunokompromitovaných pacientov pri urosepse. Urol. List 10: 37–40.Search in Google Scholar
Koga V.L., Tomazetto G., Cyoia P.S., Neves M.S., Vidotto M.C., Nakazato G. & Kobayashi R.K.T. 2014. Molecular screening of virulence genes in extraintestinal pathogenic Escherichia coli isolates from human blood culture in Brasil. BioMed Res. Int. 2014: 465054.10.1155/2014/465054Search in Google Scholar PubMed PubMed Central
López-Banda D.A., Carrillo-Casas E.M., Leyva-Leyva M., Orozco-Hoyuela G., Manjarrez-Hernández A.H., Arroyo-Escalante S., Moncada-Barrón D., Villanueva-Recillas S., Xicohtencatl-Cortes J. & Hernández-Castro R. 2014. Identification of virulence factors genes in Escherichia coli isolates from women with urinary tract infection in Mexico. BioMed. Res. Int. 2014: 959206.10.1155/2014/959206Search in Google Scholar PubMed PubMed Central
Maroncle N.M., Sivick K.E., Brady R., Stokes F.E. & Mobley H.L.T. 2006. Protease activity, secretion, cell entry, cytotoxicity, and cellular targets of secreted autotransporter toxin of uropathogenic Escherichia coli. Infect. Immun. 74: 6124–6134.10.1128/IAI.01086-06Search in Google Scholar PubMed PubMed Central
Miajlovic H. & Smith S.G. 2014. Bacterial self-defence: how Escherichia coli evades serum killing. FEMS Microbiol. Lett. 345: 1–9.10.1111/1574-6968.12419Search in Google Scholar PubMed
Mohajeri P., Khademi H., Ebrahimi R., Farhani A. & Rezaei M. 2014. Frequency distribution of virulence factors in uropathogenic Escherichia coli isolated from Kermanshah in 2011-2012. Int. J. Appl. Basic. Med. Res. 4: 111–116.10.4103/2229-516X.136794Search in Google Scholar PubMed PubMed Central
Moulin-Schouleur M., Schouler C., Tailliez P., Kao M.R., Brée A., Germon P., Oswald E., Mainil J., Blanco M. & Blanco J. 2006. Common virulence factors and genetic relationships between O18:k1:h7 Escherichia coli isolates of human and avian origin. J. Clin. Microbiol. 44: 3484–3492.10.1128/JCM.00548-06Search in Google Scholar PubMed PubMed Central
Mulvey M.A., Schilling J.D., Martinez J.J. & Hultgren S.J. 2000. Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate hots defences. Proc. Natl. Acad. Sci. USA 97 : 8829–8835.10.1073/pnas.97.16.8829Search in Google Scholar PubMed PubMed Central
Navarro-Garcia F., Gutierrez-Jimenez J., Garcia-Tovar C., Castro L.A., Salazar-Gonzalez H. & Cordova V. 2010. Pic, an autotransporter protein secreted by different pathogens in the Enterobacteriaceae family, is a potent mucus secretagogue. Infect. Immun. 78: 4101–4109.10.1128/IAI.00523-10Search in Google Scholar
Naves P., del Prado G., Huelves L., Gracia M., Ruiz V., Blanco J., Dahbi G., Blanco M., del Carmen Ponte M. & Soriano F. 2008. Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microb. Pathog. 45: 86–91.10.1016/j.micpath.2008.03.003Search in Google Scholar
Orth D., Grif K., Dierich M.P. & Würzner R. 2006. Cytolethal distending toxin in Shiga toxin-producing Escherichia coli : alleles, serotype distribution and biological effects. J. Med. Microbiol. 55: 1487–1492.10.1099/jmm.0.46666-0Search in Google Scholar
Restieri C., Garriss G., Locas M.C. & Dozois C.M. 2007. Autotransporter-encoding sequence are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl. Environ. Microbiol. 73: 1553–1562.10.1128/AEM.01542-06Search in Google Scholar
Ruiz J., Simon K., Horcajada J.P., Velasco M., Barranco M., Roig G., Moreno-Martínez A., Martínez J.A., Jiménez de Anta T., Mensa J. & Vila J. 2002. Difference in virulence factors among clinical isolates of Escherichia coli causing cystitis and pyelonephritis in women and prostatitis in men. J. Clin. Microbiol. 40: 4445–4449.10.1128/JCM.40.12.4445-4449.2002Search in Google Scholar
Sarkar S., Ulett G.C., Totsika M., Phan M.D., Schembri M.A. 2014. Role of capsule and O antigen in the virulence of uropathogenic Escherichia coli. PloS One 9: e94786.10.1371/journal.pone.0094786Search in Google Scholar
Spurbeck R.R. & Mobley H.L.T. 2013. Uropathogenic Escherichia coli, pp. 499–521. In: Donnenberg M.S. (ed.)Escherichica coli. Pathotypes and Principles of Pathogenesis. Elsevier, ISBN 978-0-12-397048-0.Search in Google Scholar
Stamm W.E. 2002. Scientific and clinical challenges in the management of urinary tract infections. Am. J. Med. 113: 1–4.10.1016/S0002-9343(02)01053-7Search in Google Scholar
Subashchandrabose S. & Mobley H.L.T. 2015. Virulence and fitness determinants of uropathogenic Escherichia coli. Microbiol. Spectr. 3: DOI: 10.1128/microbiolspec.UTI-0015-2012.10.1128/microbiolspec.UTI-0015-2012.Search in Google Scholar
Torres A., Perna N.T., Burland V., Ruknudin A., Blattner F.R. & Kaper J.B. 2002. Characterization of Cah, a calcium-binding and heat extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol. Microbiol. 45: 951–966.10.1046/j.1365-2958.2002.03094.xSearch in Google Scholar PubMed
Tóth I., Hérault F., Beutin L. & Oswald E. 2003. Production of cytolethal distending toxin by pathogenic Escherichia coli strains isolated from human and animal sources: establishment of the existence of a new cdt variant (Type IV). J. Clin. Microbiol. 41: 4285–4291.10.1128/JCM.41.9.4285-4291.2003Search in Google Scholar PubMed PubMed Central
Usein C.R., Damian M., Tatu-Chitoiu D., Capusa C., Fagaras R., Tudorache D., Nica M. & Le Bouguénec C. 2001. Prevalence of virulence genes in Escherichia coli strains isolated from Romanian adult urinary tract infection cases. J. Cell. Mol. Med. 5: 303–310.10.1111/j.1582-4934.2001.tb00164.xSearch in Google Scholar PubMed PubMed Central
Vollmerhausen T.L. & Katouli M. 2014. Molecular characterisation of Escherichia coli isolates from hospitalised children and adults with urinary tract infections. Eur. J. Clin. Microbiol. Infect. Dis. 33: 975–982.10.1007/s10096-013-2035-1Search in Google Scholar PubMed
Welch R.A. 2016. Uropathogenic Escherichia coli -associated exotoxins. Microbiol. Spectr. 4: DOI: 10.1128/microbiolspec. UTI-0011-2012.10.1128/microbiolspec. UTI-0011-2012.Search in Google Scholar
Wiles J.T., Kulesus R.R. & Mulvey M.A. 2008. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp. Mol. Pathol. 85: 11–19.10.1016/j.yexmp.2008.03.007Search in Google Scholar PubMed PubMed Central
Yamamoto S., Terai A., Yuri K., Kurazono H., Takeda Y. & Yoshida O. 1995. Detection of virulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunol. Med. Microbiol. 12: 85–90.10.1111/j.1574-695X.1995.tb00179.xSearch in Google Scholar PubMed
Yun K.W., Kim H.Y., Park H.K., Kim W. & Lim S.I. 2014. Virulence factors of uropathogenic Escherichia coli of urinary tract infection and asymptomatic bacteriuria in children. J. Microbiol. Immunol. Infect. 47: 455–461.10.1016/j.jmii.2013.07.010Search in Google Scholar PubMed
© 2017 Institute of Molecular Biology, Slovak Academy of Sciences
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