Virulence factors of Escherichia coli: an overview of animal and human infections with emphasis in bovine mastitis

Simony Trevizan Guerra, Carolina Lechinski de Paula, Carmen Alicia Daza Bolaños, Rodrigo Tavanelli Hernandes, Márcio Garcia Ribeiro


Escherichia coli is a normal inhabitant of the enteric microflora of human and animal. Intestinal and extra-intestinal infections caused by E. coli in mammals are characterized by the presence of diversity of virulence factors. In addition it can be isolated from environment surrounding human and animal farms. E. coli is the main environmental pathogen causing clinical mastitis in dairy cattle. It causes a wide range of disease severity, from changes seen exclusively in milk to severe systemic signs. The severity of clinical mastitis has been conventionally classified into three levels: mild (grade 1), moderate (score 2), and severe (score 3). Recently, reports of cases of bovine mastitis caused by environmental agents have been on the rise, in particular in countries that have succeeded in controlling contagious microorganisms. Unlike enteric and certain extra-enteric conditions in domestic animals and humans, the impact of virulence factors on the occurrence of bovine mastitis due to E. coli, as well as the clinical severity of the cases, is not fully understood. In this regard, the present study reviewed the most relevant virulence factors of E. coli in human and animals, with emphasis in bovine mastitis.


Mammary gland; Virulence properties; Coliform mastitis

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ANDERSON, G. G.; PALERMO, J. J.; SCHILLING, J. D.; ROTH, R.; HEUSER, J.; HULTGREN, S. J. Intracellular bacterial biofilm-like pods in urinary tract infections. Science, Washington, DC, v. 301, n. 5629, p. 105-107, 2003. DOI: 10.1126/science.1084550

BARROW, P. A.; HILL, A. W. The virulence characteristics of strains of Escherichia coli isolated from cases of bovine mastitis in England and Wales. Veterinary Microbiology, Barcelona, v. 20, n. 1, p. 35-48, 1989. DOI: 10.1016/0378-1135(89)90005-9

BHAKDI, S.; BAYLEY, H.; VALEVA, A.; WALEV, I.; WALKER, B.; WELLER, U.; KEHOE, M.; PALMER, M. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Archives of Microbiology, Heidelberg, v. 165, n. 2, p. 75-79, 1996. DOI: 10.1007/s002030050

BIAN, Z.; BRAUNER, A.; NORMARK, S. Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. Journal of Infectious Diseases, Oxford, v. 181, n. 2, p. 602-612, 2000. DOI: 10.1086/315233

BRADLEY, A. J. Bovine mastitis: an envolving disease. The Veterinary Journal, Bristol, v. 164, n. 2, p. 116-128, 2002. DOI: 10.1053/tvjl.2002.0724

BURVENICH, C.; VAN MERRIS, V.; MEHRZAD, J.; DIEZ-FRAILE, A.; DUCHATEAU, L. Severity of E. coli mastites is mainly determined by cow factors. Veterinary Reserch, Ohio, v. 35, n. 5, p. 521-564, 2003. DOI: 10.1051/vetres.2003023

CAPRIOLI, A.; NIGRELLI, A.; GATTI, R.; ZAVANELLA, M.; BLANDO, A. M.; MINELLI, F.; DONELLI, G. Characterisation of verocytotoxin-producing Escherichia coli isolated from pigs and cattle in northern Italy. Veterinary Record, London, v. 133, n. 13, p. 323-324, 1993. PMID: 8236671.

CHAHALES, P.; THANASSI, D. G. Structure, function, and assembly of adhesive organelles by uropathogenic bacteria. Microbiology Spectrum, Bethesda, v. 3, n. 5, p. 1-68, 2016. DOI: 10.1128/microbiolspec.UTI-0018-2013

CLERMONT, O.; BONACORSI, S.; BINGEN, E. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology, Washington, v. 66, n. 10, p. 4555-4558, 2000. DOI: 10.1128/AEM.66.10.4555-4558.2000

CLERMONT, O.; CHRISTENSON, J. K.; DENAMUR, E.; GORDON, D. M. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environmental Microbiology Reports, London, v. 5, n. 5, p. 58-65, 2013. DOI: 10.1111/1758-2229.12019.

CORRÊA, M. G. P.; MARIN, J. M. O-serogroups, eae gene and EAF plasmid in Escherichia coli isolates from cases of bovine mastitis in Brazil. Veterinary Microbiology, Barcelona, v. 85, n. 2, p. 125-132, 2002. DOI: 10.1016/S0378-1135(01)00413-8

CROXEN, M. A.; FINLAY, B. B. Molecular mechanisms of Escherichia coli pathogenicity. Nature Reviews Microbiology, London, v. 8, n. 1, p. 26-38, 2010. DOI: 10.1038/nrmicro2265

DÖPFER, D.; ALMEIDA, R. A.; LAM, T. J. G. M.; NEDERBRAGT, H.; OLIVER, S. P.; GAASTRA, W. Adhesion and invasion of Escherichia coli from single and recurrent clinical cases of bovine mastitis in vitro. Veterinary Microbiology, Barcelona, v. 74, n. 4, p. 331-343, 2000. DOI: 10.1016/S0378-1135(00)00191-7

EWERS, C.; LI, G.; WILKING, H.; KIEBLING, S.; ALT, K.; ANTÁO, E. M.; LATURNUS, C.; DIEHL, I.; GLODDE, S.; HOMEIER, T.; BÖHNKE, U.; STEINRÜCK, H.; PHILIPP, H-C.; WIELER, L. H. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? International Journal of Medical Microbiology, Berlin, v. 297, n. 3, p. 163-176, 2007. DOI: 10.1016/j.ijmm.2007.01.003

FERNANDES, J. B. C.; ZANARDO, L. G.; GALVÃO, N. N.; CARVALHO, I. A.; NERO, L. A.; MOREIRA, M. A. S. Escherichia coli from clinical mastitis serotypes and virulence factors. Journal of Veterinary Diagnostic Investigation, Ontario, v. 23, n. 6, p. 1146-1152, 2011. DOI: 10.1177/1040638711425581

GERBER, A.; KARCH, H.; ALLERBERGER, F.; VERWEYEN, H. M.; ZIMMERHACKL, L. B. Clinical course and the role of Shiga toxin producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997-2000, in Germany and Austria: a prospective study. Journal of Infectious Diseases, Oxford, v. 186, n. 4, p. 493-500, 2002. DOI: 10.1086/341940

GUERRA, S. T.; DALANEZI, F. M.; PAULA, C. L. de; HERNANDES, R. T.; PANTOJA, J. C. F. P.; LISTONI, F. P.; LANGONI, H.; RIBEIRO, M. G. Putative virulence factors of extra-intestinal Escherichia coli isolated from bovine mastitis with different clinical scores. Letters in Applied Microbiology, Cardiff, v. 68, v.68, n. 5, p. 403-408, 2019. DOI: 10.1111/lam.13113

GÜLER, L.; GÜNDÜZ, K. Virulence properties of Escherichia coli isolated from clinical bovine mastitis. Turkish Journal of Veterinary and Animal Sciences, Akai Cadessi, v. 31, n. 5, p. 361-365, 2007.

HAHN, E.; WILD, P.; HERMANNS, U.; SEBBEL, P.; GLOCKSHUBER, R.; HÄNER, M.; TASCHNER, N.; BURKHARD, P.; AEBI, U.; MÜLLER, S. A. Exploring the 3D molecular archicture of Escherichia coli type 1 pili. Journal of Molecular Biology, Free acess online, v. 323, n. 5, p. 845-857, 2002. DOI: 10.1016/S0022-2836(02)01005-7

HANTKE, K.; NICHOLSON, G.; RABSCH, W.; WINKELMANN, G. Salmochelins, siderophores of Salmonella entérica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proceedings of National Academy of Sciences, Berkeley, v. 100, n. 7, p. 3677-3682, 2003. DOI: 10.1073/pnas.0737682100

HENDERSON, I. R.; NATARO, J. P. Virulence functions of autotransporter proteins. Infection and Immunity, Washington, v. 69, n. 3, p. 1231-1243, 2001. DOI: 10.1128/IAI.69.3.1231-1243.2001

HOGAN, J.; SMITH, K. L. Coliform mastitis. Veterinary Research, Ohio, v. 34, n. 5, p. 507-519, 2003. DOI: 10.1051/vetres:2003022

HUANG, S. H.; WASS, C.; FU, Q.; PRASADARAO, N. V.; STINS, M.; KIM, K. S. Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infection and Immunity, Washington, v. 63, n. 11, p. 4470-4475, 1995.

JOHNSON, J. R.; MURRAY, A. C.; GAJEWSKI, A.; SULLIVAN, M.; SNIPPES, P.; KUSKOWSKI, M. A.; SMITH, K. E. Isolation and molecular characterization of Nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrobial Agents and Chemotherapy, Washington, v. 47, n. 7, p. 2161-2168, 2003. DOI: 10.1128/AAC.47.7.2161-2168.2003

JOHNSON, J. R.; RUSSO, T. A.; TARR, P. I.; CARLINO, U.; BILGE, S. S.; VARY, J. C. Molecular epidemiological and phylogenetic associations of two novel putative virulence genes, iha and iroN (E. coli), among Escherichia coli isolates from patients with urosepsis. Infection and Immunity, Washington, v. 68, n. 5, p. 3040-3047, 2000. DOI: 10.1128/IAI.68.5.3040-3047.2000

KAIPAINEN, T.; POHJANVIRTA, T.; SHPIGEL, N. Y. Virulence factors of Escherichia coli isolated from bovine clinical mastitis. Veterinary Microbiology, Barcelona, v. 85, n. 1, p. 37-46, 2002. DOI: 10.1016/S0378-1135(01)00483-7

KAPER, J. B.; NATARO, J. P.; MOBLEY, H. L. T. Pathogenic Escherichia coli. Nature Reviews Microbiology, v. 2, n. 2, p. 123–140, 2004. DOI: 10.1038/nrmicro818

KJAERGAARD, K.; HASMAN, H.; SCHEMBRI, M. A.; KLEMM, P. Antigen 43-mediated autotransporter display, a versatile bacterial cell surface presentation system. Journal of Bacteriology, Washington, v. 184, n. 15, p. 4197-4204, 2002. DOI: 10.1128/JB.184.15.4197-4204.2002

KLEMM, P.; HANCOCK, V.; SCHEMBRI, M. A. Fimbrial adhesins from extraintestinal Escherichia coli. Environmental Microbiology Reports, London, v. 2, n. 5, p. 628-640, 2010. DOI: 10.1111/j.1758-2229.2010.00166.x

KLEMM, P.; SCHEMBRI, M. A. Bacterial adhesins: function and structure. International Journal of Medical Microbiology, Amsterdã, v. 290, n. 1, p. 27-35, 2000. DOI: 10.1016/S1438-4221(00)80102-2

KLEMM, P.; SCHEMBRI, M. Type 1 fimbriae, curli, and antigen 43: adhesion, colonization, and biofilm formation. EcoSal Plus, Cambridge, v. 1, n. 1, p. 1-18, 2004. DOI: 10.1128/ecosalplus.

KLINE, K. A.; FÄLKER, S.; DAHLBERG, S.; NORMARK, S.; HENRIQUES-NORMARK, B. Bacterial adhesins in host-microbe interaction. Cell Host & Microbe, Amsterdã, v. 5, n. 6, p. 580-592, 2009. DOI: 10.1016/j.chom.2009.05.011

KÖHLER, C.; DOBRINDT, U. What defines extraintestinal pathogenic Escherichia coli? International Journal of Medical Microbiology, Amsterdã, v. 301, n.8, p. 642-647, 2011. DOI: 10.1016/j.ijmm.2011.09.006

KÖSTER, W. ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B 12. Research in Microbiology, Amsterdã, v. 152, n. 3-4, p. 291-301, 2001. DOI: 10.1016/S0923-2508(01)01200-1

LE BOUGUÉNEC, C. Adhesins and invasins of pathogenic Escherichia coli. International Journal of Medical Microbiology, Amsterdã, v. 295, n. 6, p. 471-478, 2005. DOI: 10.1016/l.ijmm.2005.07.001

LINTON, A. H.; HOWE, K.; SOJKA, W. J.; MAFF, C. W. A note on the range of Escherichia coli O-serotypes causing clinical bovine mastitis and their antibiotic resistance spectra. Journal of Applied Bacteriology, London, v. 46, n. 3, p. 585-590, 1979. DOI: 10.1111/j.1365-2672.1979.tb00859.x

LIPMAN, L. J. A.; NIJS, A.; GAASTRA, W. Isolation and identification of fimbriae and toxin production by Escherichia coli strains from cows with clinical mastitis. Veterinary Microbiology, Barcelona, v. 47, n. 1, p. 1-7, 1995. DOI: 10.1016/0378-1135(95)00108-M

LIU, Y.; LIU, G.; LIU, W.; LIU, Y.; ALI, T.; CHEN, W.; YIN, J.; HAN, B. Phylogenetic group, virulence factors and antimicrobial resistance of Escherichia coli associated with bovine mastitis. Research in Microbiology, Amsterdã, v. 165, n. 4, p. 273-277, 2014. DOI: 10.1016/j.resmic.2014.03.007

MOMTAZ, H. Investigation of virulence factors in Escherichia coli isolated from clinical and subclinical bovine mastitis. Bulgarian Journal of Veterinary Medicine, Stara Zagora, v. 13, n. 2, p. 122-126, 2010.

MOMTAZ, H.; DEHKORDI, F. S.; TAKTAZ, T.; REZVANI, A.; YARALI, S. Shiga toxin-producing Escherichia coli isolated from bovine mastitic milk: serogroups, virulence factors, and antibiotic resistance properties. The Scientific World Journal, New York, v. 2012, n. 1, p. 1-9, 2012. DOI: 10.1100/2012/618709

MYSOREKAR, I. U.; HULTGREN, S. J. Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proceedings of the National Academy of Sciences, St. Loius, v. 103, n. 38, p. 14170-14175, 2006. DOI: 10.1073/pnas.0602136103

NEMETH, J.; MUCKLE, C. A.; GYLES, C. L. In vitro comparison of bovine mastitis and fecal Escherichia coli isolates. Veterinary Microbiology, Barcelona, v. 40, n. 3, p. 231-238, 1994. DOI: 10.1016/0378-1135(94)90112-0

OLIVEIRA, C. S. F.; HOGVEEN, H.; BOTELHO, A. M.; MAIA, P. V.; COELHO, S. G.; HADDAD, J. P. A. Cow-specific risk factors for clinical mastitis in Brazilian dairy cattle. Preventive Veterinary Medicine, Colorado, v. 121, n. 3-4, p. 297-305, 2015. DOI: 1o.1016/j.prevetmed.2015.08.001

PINZÓN-SÁNCHEZ, C.; RUEGG, P. L. Risk factors associated with short-term post-treatment outcomes of clinical mastitis. Journal of Dairy Science, Champaign, v. 94, n. 7, p. 3397-3410, 2011. DOI: 10.3168/jds.2010-3925

PRASADARAO, N. V.; WASS, C. A.; HACKER, J.; JANN, K.; KIN, K. S. Adhesion of S-fimbriated Escherichia coli to brain glycolipids mediated by sfaA gene-encoded protein of S-fimbriae. The Journal of Biological Chemistry, Maryland, v. 268, n. 14, p. 10356-10363, 1993.

PROFT, T.; BAKER, E. N. Pili in Gram-negative and Gram-positive bacteria-structure, assembly and their role in disease. Cellular and Molecular Life Sciences, Heidelberg, v. 66, n. 4, p. 613-635, 2009. DOI: 10.1007/s00018-008-8477-4

PROVENCE, D. L.; CURTISS, R. Role of crl in avian pathogenic Escherichia coli: a knockout mutation of crl does not affect hemagglutination activity, fibronectin binding, or curli production. Infection and Immunity, Washington, v. 60, n. 11, p. 4460-4467, 1992.

RAETZ, C. R. H.; WHITFIELD, C. Lipopolysaccharide Endotoxins. Annual Review of Biochemistry, Palo Alto, v. 71, n. 1, p. 635-700, 2002. DOI: 10.1146/annurev.biochem.71.110601.135414

RIBEIRO, M. G.; COSTA, E. O.; LEITE, D. S.; LANGONI, H.; GARINO JÚNIOR, F.; VICTÓRIA, C.; LISTONI, F. J. P. Fatores de virulência em linhagens de Escherichia coli isoladas de mastite bovina. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v. 58, n. 5, p. 724-731, 2006. Disponível em: Acesso em: 29 maio 2019.

RIBEIRO, M. G.; LEITE, D. S.; SIQUEIRA, A. K. Enfermidades por Escherichia coli. In: MEGID, J.; RIBEIRO, M. G.; PAES, A. C. Doenças infecciosas em animais de produção e companhia. Rio de Janeiro: Roca, 2016. p. 243-273.

RIETSCHEL, E. T.; KIRIKAE, T.; SCHADE, F. U.; MAMAT, U.; SCHMIDT, G.; LOPPNOW, H.; ULMER, A. J.; ZAHRINGER, U.; SEYDEL, U.; DI PADOVA, F. Bacterial endotoxin: molecular relationships of structure to activity and function. The FASEB Journal, Bethesda, v. 8, n. 2, p. 217-225, 1994. DOI: 10.1096/fasebj.8.2.8119492

RODRIGUEZ-SIEK, K. E.; GIDDINGS, C. W.; DOETKOTT, C.; JOHNSON, T. J.; NOLAN, L. K. Characterizing the APEC pathotype. Veterinary Research, Ohio, v. 36, n. 2, p. 241-256, 2005. DOI:10.1051/vetres:2004057

RUEGG, P. L. A 100-year review: mastitis detection, management, and prevention. Journal of Dairy Science, Champaign, v. 100, n. 12, p. 10381-10397, 2017. DOI: 10.3168/jds.2017.13023

SCHEMBRI, M. A.; HJERRILD, L.; GJERMANSEN, M.; KLEMM, P. Differential expression of the Escherichia coli autoaggregation factor antigen 43. Journal of Bacteriology, Washington, v. 185, n. 7, p. 2236-2242, 2003. DOI: 10.1128/JB.185.7.2236-2242

SHPIGEL, N. Y.; ELAZAR, S.; ROSENSHINE, I. Mammary pathogenic Escherichia coli. Current Opinion in Microbiology, Amsterdã, v. 11, n. 1, p. 60-65, 2008. DOI: 10.1016/j.mib.2008.01.004

SHUSTER, D. E.; HARMON, R. J.; JACKSON, J. A.; HEMKEN, R. W. Suppression of milk production during endotoxin-induced mastitis. Journal of Dairy Science, Champaign, v. 74, n. 11, p. 3763-3774, 1991. DOI: 10.3168/jds.S0022-0302(91)78568-8

STEPHAN, R.; KUHN, K. Prevalence of verotoxigenic-producing Escherichia coli (VTEC) in bovine E. coli mastitis and their antibiotic resistance patterns. Zentralblatt Veterinarmed, Berlin, v. 46, n. 6, p. 423-427, 1999.

SUOJALA, L.; POHJANVIRTA, T.; SIMOJOKI, H.; MYLLYNIEMI, A. L.; PITKÄLÄ, A.; PELKONEN, S.; PYÖRÄLÄ, S. Phylogeny, virulence factors and antimicrobial susceptibility of Escherichia coli isolated in clinical bovine mastitis. Veterinary Microbiology, Barcelona, n. 147, n. 3-4, p. 383-388, 2011. DOI: 10.1016/j.vetmic.2010.07.011

TARR, P. I.; GORDON, C. A.; CHANDLER, W. L. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. The Lancet, Amsterdã, v. 365, n. 9464, p. 1073-1086, 2005. DOI: 10.1016/S0140-6736(05)71144-2

TÓTH, I.; HÉRAULT, F.; BEUTIN, L.; OSWALD, E. Production of cytolethal distending toxins by pathogenic Escherichia coli strains isolated from human and animal sources: establishment of the existence of a new cdt variant (Type IV). Journal of Clinical Microbiology, Barcelona, v. 41, n. 9, p. 4285-4291, 2003. DOI: 10.1128/JCM.41.9.4285-4291.2003

VAN BOST, S.; MAINIL, J. Facteurs de virulence et propriétés spécifiques des souches invasives d’Escherichia coli: lll) Production de toxines. Annales de Médecine Vétérinaire, Liège, v. 147, n. 1, p. 327-342, 2003. Available at: Accessed at: 29 may 2019.

WENZ, J. R.; BARRINGTON, G. M.; GARRY, F. B.; DINSMORE, R. P.; CALLAN, R. J. Use of systemic disease signs to assess disease severity in dairy cows with acute coliform mastitis. Journal of the American Veterinary Medical Association, Schaumburg, v. 218, n. 4, p. 567-572, 2001. DOI: 10.2460/javma.2001.218.567

WENZ, J. R.; BARRINGTON, G. M.; GARRY, F. B.; ELLIS, R. P.; MAGNUSON, R. J. Escherichia coli isolates serotypes, genotypes and virulence genes and clinical coliform mastitis severity. Journal of Dairy Science, Champaign, v. 89, n. 9, p. 3408-3412, 2006. DOI: 10.3168/jds.S0022-0302(06)72377-3

WILLIAMS, D. M.; SREEDHAR, S. S.; MICHELL, J. J.; CHAN, J. C. M. Acute kidney failure: a pediatric experience over 20 years. Archives of Pediatrics & Adolescent Medicine, Chicago, v. 156, n. 9, p. 893-900, 2002. DOI: 10.1001/archpedi.156.9.893


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