Extra-intestinal pathogenic Escherichia coli – threat connected with food-borne infections
More details
Hide details
Department of Microbiology, National Veterinary Research Institute, Puławy, Poland
Bernard Wasiński   

National Veterinary Research Institute, Partyzantów 57, 24-100, Puławy, Poland
Infections caused by extra-intestinal pathogenic Escherichia coli (ExPEC) are a serious public health problem worldwide. The most troublesome are urinary tract infections, severe neonatal meningitis, serious intraabdominal infections, and more rarely, pneumonia, intravascular-device infections, osteomyelitis, soft-tissue infections or sometimes bacteraemia. These strains are also able cause significant economic losses in animal husbandry. A thorough understanding of ExPEC ecology, reservoirs, chains and dynamics of transmission can greatly contribute to a reduction in the burden of ExPEC-associated disease. The ability of E. coli (including ExPEC) to exist and survive in various ecological niches impedes the precise recognition and indication of transmission routes most important for individual infections cases. Among many identified ExPEC reservoirs, animal companion and animals providing food seem to be important sources of infection for human; however, the real level of risk connected with potential transmission of these bacteria remains unclear. Food is indicated as one of potential ways of transmission. Despite a quite high number of reports, many of the uncertainties are expected to be reliably elucidated. This review presents most important data on the current state of knowledge concerning the potential role of food in ExPEC transmission. The possible consequences of ExPEC infections in human and animals are briefly described.
Poolman JT, Wacker M. Extraintestinal pathogenic Escherichia coli, a common human pathogen: challenges for vaccine development and progress in the field. J I D. 2016; 213: 6–13.
Singer RS. Urinary tract infections attributed to diverse ExPEC strains in food animals: evidence and data gaps. Front Microbiol. 2015; 6: 28. doi:10.3389/fmicb.2015.00028.
Dobrindt U, Hacker J. Targeting virulence traits: potential strategies to combat extraintestinal pathogenic E. coli infections. Curr Opin Microbiol. 2008; 11: 409–413.
Manges AR. Escherichia coli and urinary tract infections: the role of poultry meat. Clin Microbiol Infect. 2016; 22: 122–129.
Russo TA, Johnson JR. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J I D. 2000; 181: 1753–1754.
Manges A, Johnson J. Reservoirs of extraintestinal pathogenic Escherichia coli. Microbiol Spectrum 2015; 3(5): UTI-0006-2012. doi:10.1128/microbiolspec.UTI-0006-2012.
Clermont O, Christensen JK., Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revised: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep. 2013; 5: 58–65.
Markland SM, LeStrange KJ, Sharma M, Kniel KE. Old friends in new places: exploring the role of extraintestinal E. coli in intestinal disease and foodborne illness. Zoonoses and Public Health 2015; 62: 491–496.
Bélanger L, Garenaux A, Harel J, Boulianne M, Nadeau E, Dozois CM. Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli. FEMS Immuno Med Microbiol. 2011; 62: 1–10.
Yamamoto S. Molecular epidemiology of uropathogenic Escherichia coli. J Infect Chemother. 2007; 13: 68–73.
Bonacorsi S, Bingen E. Molecular epidemiology of Escherichia coli causing neonatal meningitis. Int J Med Microbiol. 2005; 295: 373–381.
Mellata M. Human and avian extraintestinal pathogenic Escherichia coli: infections, zoonotic risk and antibiotic resistance trends. Foodborn Pathogens and Disease 2013; 10: 916–932.
Fairbrother JM, Gyles C. Colibacillosis. In: Diseases of swine (2012) 10 th edn. Edited by Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ and Stevenson GW. (ed.) Ames, Chichester, Oxford: John Wiley & Sons 723–749.
Tan C, Xu ZA, Zheng H, Liu W, Tang X, Shou J, Wu B, Wang S, Zhao G, Chen H. Genome sequence of porcine extraintestinal pathogenic Escherichia coli strain. J Bacteriol. 2011; 193: 5038.
DebRoy C, Roberts EJayarao B, Brooks J. Bronchopneumonia associated with extraintestinal pathogenic Escherichia coli in a horse. J Vet Diagn Invest. 2008; 20: 661–664.
Breitschwerdt EB, DebRoy C, Mexas AM, Brown TT, Remich AK. Isolation of necrotoxogenic Escherichia coli from a dog with hemorrhagic pneumonia. J Am Vet Med Assoc. 2005; 226: 2016–2019.
Hndt LK, Stoffergen DA, Prescott JS, Pouch WJ, Ngai DT, Anderson CA, Gatto NT, DebRoy C, Fairbrother JM, Motzel SM, Klein HJ. Clinical and microbiologic characterization of hemorrhagic pneumonia due to extraintestinal pathogenic Escherichia coli in four young dogs. Comp Med. 2003; 53: 663–670.
Snyder JA, Haugen BJ. Coordinate expression of fimbriae in uropathogenic Escherichia coli. Infect Immun. 2005; 73: 7588–7596.
Sura R, Van Kruingen HJ, DebRoy C, Hinckley LS, Greenberg KJ, Gordon Z, French RA. Extraintestinal pathogenic Escherichia coli induced acute necrotizing pneumonia in cats. Zoonoses Public Health 2007; 54: 307–313.
Ender PT, Gajana D, Johnston B, Clabots C, Tamarkin FJ, Johnson JR. Transmission of an Extended-Spectrum-Beta-Lactamase-producing Escherichia coli (sequence type ST131) strain between the father and daughter resulting in septic shock and emphysematous pyelonephritis. J Clin Microbiol. 2009; 47: 3780–3782.
Foxman B, Zhang L, Tallman P, Andree BC, Geiger AM, Koopman JS, Gillespie BW, Palin KA, Sobel JD, Rode CK, Bloch CA, Marrs CF. Transmission of uropathogens between sex partners. J Infect Dis. 1997; 175: 989–992.
Johnson JR, Clabots C. Sharing of virulent Escherichia coli clones among household members of a woman with acute cystitis. Clin Infect Dis. 2006; 43: 101–108.
Uleryd P, Sandberg T, Scheutz F, Clabots C, Johnston BD, Thuras P, Johnson JR. Colonization with Escherichia coli strains among female sex partners of men with febrile urinary tract infection. J Clin Microbiol. 2015; 53: 1947–1950.
Jakobsen L, Hammerum AM, Frimodt-Møller N. Detection of clonal group A Escherichia coli isolates from broiler chickens, broiler chicken meat, community-dwelling humans, and urinary tract infection (UTI) patients and their virulence in a mouse UTI model. Appl Environ Microbiol. 2010; 76: 8281–8284.
Johnson JR, Delavari P, O’Bryan TT, Smith K.E, Tatini S. Contamination of retail foods, particularly turkey, from community markets (Minnesota 1999–2000) with antimicrobial-resistant and extraintestinal pathogenic Escherichia coli. Foodborne Path Dis. 2005; 2: 38–49.
Leverstein-van Hall M, Dierikx CM, CohenStuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, Platteel T, Fluit AC, van de Sande-Bruinsma N, Scharinga J, Bonten MJM, Mevius DJ. Dutch patients, retail meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect. 2011; 17: 873–880.
Overdevest I, Willemsen I, Rijnsburger M, Eustance A, Xu L, Hawkey P.,Heck M, Savelkoul P, Vandenbroucke-Grauls C, van der Zwaluw K, Huijsdens X, Kluytmans J. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emarg Infect Dis. 2011; 17: 1216–1222.
Ukah UV, Glass M, Avery B, Daignault D, Mulvey MR, Reid-Smith RJ, Parmley EJ, Portt A, Boerlin P, Manges AR. Risk factors of acquisition of multidrug-resistant Escherichia coli and development of community-acquired urinary tract infections. Epidemiol Infect. 2018; 146: 46–57.
Jakobsen L, Spangholm DJ, Pedersen K, Jansen LB, Emborg HD, Agersø Y, Aarestrup FM, Hammerum AM, Frimodt-Møller N. Broiler chicken, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients. Int J Food Microbiol. 2010; 142: 264–272.
Manges AR, Smith SP, Lau BJ, Nuval CJ, Eisenberg JN, Dietrich PS, Riley LW. Retail meat consumption and the acquisition of antimicrobial resistant Escherichia coli causing urinary tract infections: a case-control study. Foodborne Pathog Dis. 2007; 4: 419–431.
Xia X, Meng J, Zhao S, Bodies-Jones S, Gaines S.A, Ayres SL, McDermott PF. Identification of antimicrobial resistance of extraintestinal pathogenic Escherichia coli from retail meat. J Food Protect. 2011; 74: 38–44.
Vincent C, Boerlin P, Diagnault D, Dozois CM, Dutil L, Galanakis C, Reid-Smith RJ, Tellier PP, Tellis PA, Ziebell K, Manges AR. Food reservoir for Escherichia coli causing urinary tract infections. Emerg Infect Dis. 2010; 16: 88–95.
Mora A, Herrera A, Mamani R, López C, Alonso MP, Blanco JE, Blanco M, Dahbi G, García-Garrote F, Pita JM, Coira A, Bernárdez MI, Blanco J. Recent emergence of clonal group O25b:K1:H4-B2-ST131 ibeA strains among Escherichia coli poultry isolates, including CTX-M-9-producing strains, and comparison with clinical human isolates. Appl Environ Microbiol. 2010; 76: 6991–6997.
Mora A, Lopez C, Herrera A, Viso S, Mamani R, Dhabi G, Alonso MP, Blanco M, Blanco JE, Blanco J. Emerging avian pathogenic Escherichia coli strains belonging to clonal groups O111:H4-D-ST2085 and O111:H4-D-ST117 with high virulence-gene content and zoonotic potential. Vet Microbiol. 2011; 156: 347–352.
Cortés P, Blanc V, Mora A, Dahbi G, Blanco JE, Blanco M, López C, Andreu A, Navarro F, Alonso MP, Bou G, Blanco J, Llagostera M. Isolation and characterization of potentially pathogenic antimicrobial-resistant Escherichia coli strains from chicken and pig farms in Spain. Appl Environ Microbiol. 2010; 76: 2799–2805.
Johnson TJ, Kariyawasam S, Wannemuehler Y, MangiameleP, Johnson SJ, Doetkott C, Skyberg J, Lynne AM, Johnson JR, Nolan LK. The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol. 2007; 189: 3228–3236.
Johnson TJ, Longue CM, Johnson JR, Kuskowski MA, Sherwood JS, Barnes HJ, DebRoy C, Wannemuehler YM, Obeta-Yasuoka M, Spanjaard L, Nolan LK. Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from human and poultry. Foodborne Pathol. 2012; 9: 37–46.
Johnson TJ, Wannemuehler Y, Johnson SJ, Stell AL, Doetkott C, Johnson JR, Kim KS SpanjaaL, Nolan LK. Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals mixed subset representing potential zoonotic pathogens. Appl Environ Microbiol. 2008; 74: 7043–7050.
Moulin-Schouleur M, Répérant M, Laurent S, Brée A, Mignon-Grasteau S, Germon P, Rasschaert D, Schouler C. Extraintestinal pathogenich Escherichia coli strains of avian and human origin: link between phylogenetic relationship and common virulence patterns. J Clin Microbiol. 2007; 45: 3366–3376.
Rodrigues-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Fakhr MK, Nolan LK. Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 2005; 151: 2097–2110.
Tivendale KA, Lounge CM, Kariyawasam S, Jordan D, Hussein A, Li G, Wannemuehler Y, Nolan LK. Avian pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease. Infect. Immun. 2010; 78: 3412–3419.
Manges AR, Johnson JR. Food-borne origins of Escherichia coli causing extraintestinal infections. Clin Infect Dis. 2012; 55: 712–719.
Olsen RH, Christensen H, Bisgaard M. Comparative genomics of multiple plasmids from APEC associated with clonal outbreaks demonstrates major similarities and identifies several potential vaccine-targets. Vet Microbiol. 2012; 158: 384–393.
Jakobsen L, Garneau P, Bruant P, Harel J, Olsen SS, Porsbo LJ, Hammerum AM, Frimodt-Moller N. Is Escherichia coli urinary tract infection a zoonosis? Proof of direct link with production animals and meat. Eur J Clin Microbiol Infect Dis. 2012; 31: 1121–1129.
Mellata M, Johnson JR, Curtiss III R. Escherichia coli isolates from commercial chicken meat and eggs cause sepsis, meningitis and urinary tract infection in rodent models of human infections. Zoonoses Public Health 2018; 65: 103–113.
Johnson JR, Kuskowski MA, Smith K, O’Bryan TT, Tatini S. Antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in retail foods. J Infect Dis. 2005; 191: 1040–1049.
Racicot Bergeron C, Prussing C, Boerlin P, Diagnault D, Dutil L, Reid-Smith RJ, Zhanel GG, Manges AR. Chicken as reservoir for extraintestinal pathogenic Escherichia coli in humans. Canada Emerg Infect Dis. 2012; 18: 415–421.
Agersø Y, Jensen JD, Hasman H, Pedersen K. Spread of extended spectrum cephalosporinase-producing Escherichia coli clones and plasmids from parent animals to broilers and to broiler meat in a production without of cephalosporins. Foodborne Pathog Dis. 2014;11: 740–749.
Egervanrn M, Borjesson S, Byfors S, Finn M, Kaipe C, Englund S, Lindblad M. Escherichia coli with extended-spectrum beta-lactamases or transferable AmpC β-lactamases and Salmonella on meat imported into Sewden. Int J Food Microbiol. 2014, 171, 8–14.
Lyhs U, Ikonen I, Pohjavirta T, Raninen K, Pärko-Mälelä P, Pelkonen S. Extraintestinal pathogenic Escherichia coli in poultry meat products on the Finnish retail market. Acta Vet Scand. 2012; 16: 54–64.
Literak I, Reitschmied T, Bujnakova D, Dolejska M, Cizek A, Bardon J, Pokludova L, Alexa P, Halova D, Jamborova I. Broilers as a source of quinolone-resistant and extraintestinal pathogenic Escherichia coli in the Czech Republic. Microb Drug Resist. 2013; 19: 57–63.
Sukkua K, Pomwised R, Rattanachuay P, Khianngam S, Sukhumungoon P. Characterization of extraintestinal pathogenic Escherichia coli from meat in Southern Thailand. Southeast Asian J Trop Med. Public Health 2017, 48, 98–108.
Hussain A, Shaik S, Ranjan A, Nandanwar N, Tiwari SK, Majid M, Baddam R, Qureshi IA, Semmler T, Wieler LH, Islam MA, Chakravortty D, Ahmed N. Risk of transmission of antimicrobial resistant Escherichia coli from commercial broiler and free-range retail chicken in India. Front Microbiol. 2017; Nov 13;8:2120. doi:10.3389/fmicb.2017.02120.
Kobayashi RKT, Aquino I, Ferreira ALS, Vidotto MC. EcoR phylogenetic analysis and virulence typing of avian pathogenic Escherichia coli strains and Escherichia coli isolates from commercial chicken carcasses in southern Brazil. Foodborne Pathog Dis. 2011; 8: 631–635.
Qabajah M, Awwad E, Ashhab Y. Molecular characterization of Escherichia coli from dead broiler with signs of colibacillosis and ready-to-market chicken meat in the West Bank Br Poult Sci. 2014; 55: 422–451.
Ding Y, Tang X, Lu P, Wu B, Xu Z, Liu W, Zhang R, Bei W, Chen H, Tan C. Clonal analysis and virulent traits of pathogenic extraintestinal Escherichia coli isolates from swine in China. BMC Vet Res. 2012; 8: 140.
Khan SB, Zou G, Cheng Y, Xiao R, Li L, Wu B, Zhou R. Phylogenetic grouping and distribution of virulence genes in Escherichia coli along the production and supply chain of pork around Hubei, China. J Microbiol Immunol Infect. 2017; 50: 382–385.
Trobos M, Christensen H, Sunde M, Nordentoft S, Agersø Y, Simonsen GS, Hammerum AM, Olsen JE. Characterization of sulphonamide-resistant Escherichia coli using comparison of sul2 gene sequences and multilocus sequence typing. Microbiology 2009; 155: 831–836.
Xia X, Meng J, McDermott PF, Zhao S. Escherichia coli from retail meats carry genes associated with uropathogenic Escherichia coli, but are weekly invasive in human bladder cell culture. J Appl Microbiol. 2011; 110: 1166–1176.
Schmidt JW, Agga GE, Bosilevac JM, Brichta-Harhay DM, Shackelford SD, Wang R, Wheeler TL, Arthur TM. Occurrece of antimicrobial-resistant Escherichia coli and Salmonella enterica in beef cattle production and processing continuum. Appl Environ Microbiol. 2015; 81: 713–725.
Nordstrom L, Liu CM, Price LB. Foodborne urinary tract infections: a new paradigm for antimicrobial-resistant foodborne illness. Front Microbiol. 2013; 4: 29. doi: 10.3389/fmicb.2013.00029.
Ramchandai M, Manges AR, DebRoy C, Smith SP, Johnson JR, Riley LW. Possible animal origin of human-associated multidrug-resistant, uropathogenic Escherichia coli. Clin Infect Dis. 2005; 40: 251–257.
Santo E, Rodolpho D, Marin JM. Presence of extraintestinal pathogenic Escherichia coli in butcheries in Taquaritinga, SP, Brazil. Brazil J Microbiol. 2007; 38: 591–593.
Mitchell NM, Johnson JR, Johnston B, Ourtiss R, Mellata M. Zoonotic potential of Escherichia coli isolates form retail chicken meat products and eggs. Appl Environ Microbiol. 2015; 81: 1177–1187.
Campos de ACLP, Puño-Sarmineto JJ, Medeiros LP, Gazal LES, Maluta RP, Navarro A, Kobayashi RKT, Fagan EP, Nakazato G. Virulence genes and antimicrobial resistance in Escherichia coli from cheese made from unpasteurized milk in Brazil. Foodborne Pathog Dis. 2018; 15: 94–100.
Guzman-Hernandez R, Contreras-Rodriguez A, Hernandez-Velez R, Perez-Martinez I, Lopez-Merino A, Zaidi MB, Estrada-Garcia T. Mexican unpasteurized fresh cheeses are contaminated with Salmonella, non-O157 Shiga toxin producing Escherichia coli and potential uropathogenic E. coli strains: A public health risk. Int. Food Microb. 2016; 237: 10–16.
Ribeiro LF, Barbose MM, Pinto FR, Maluta RP, Oliveira MC, de Souza V, de Medeiros MI, Borges LA, do Amaral LA, Fairbrother JM. Antimicrobial resistance and virulence factors of Escherichia coli in cheese made from unpasteurized milk in three cities in Brazil. Foodborne Pathog Dis. 2016; 13: 469–476.
Scheinberg JA, Dudley EG, Campbell J, Roberts B, DɪMarzio M, DebRoy C, Cutter CN. Prevalence and phylogenetic characterization of Escherichia coli and hygiene indicator bacteria isolated from leafy green produce, beef, and pork obtained from farmers’ markets in Pennsylvania. J Food Prot. 2017; 80: 237–244.
Sarowska J, Futom-Koloch B, Jama-Kmiecik A, Frej-Madrzak M, Ksiazczyk M, Bugl-Plaskonska G, Choroszy-Krol I. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports. Gut Pathog. 2019; 11: 10.
Vila J, Sáez-López E, Johnson JR, Römling U, Dobrindt U, Catón R, Giske GC, Naas T, Carattoli A, Martínez-Medina M, Bosch J, Retmar P, Rodríguez-Bano J, BaqueroF, Soto SM. Escherichia coli: an old friend with new tidings. FEMS Microbiol Rev. 2016; 40: 437–463.