what is the importance of escherichia coli to humans
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June 2011
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FEMS Immunology & Medical Microbiology
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Abstract
Extraintestinal pathogenic Escherichia coli (ExPEC) are an important cause of urinary tract infections, neonatal meningitis and septicaemia in humans. Animals are recognized as a reservoir for homo intestinal pathogenic East. coli, but whether animals are a source for man ExPEC is still a matter of contend. Pathologies caused past ExPEC are reported for many subcontract animals, especially for poultry, in which colibacillosis is responsible for huge losses within broiler chickens. Cases are besides reported for companion animals. Commensal E. coli strains potentially carrying virulence factors involved in the development of human pathologies also colonize the intestinal tract of animals. This review focuses on the recent prove of the zoonotic potential of ExPEC from beast origin and their potential direct or indirect transmission from animals to humans. As antimicrobials are commonly used for livestock production, infections due to antimicrobial-resistant ExPEC transferred from animals to humans could exist fifty-fifty more than hard to treat. These findings, combined with the economic impact of ExPEC in the animal production industry, demonstrate the need for adapted measures to limit the prevalence of ExPEC in animal reservoirs while reducing the use of antimicrobials as much as possible.
Introduction
Escherichia coli is a bacterial commensal of the intestinal microflora of a multifariousness of animals, including humans. Nevertheless, not all Eastward. coli strains are harmless, equally some are able to cause diseases in humans also as in mammals and birds (Dho-Moulin & Fairbrother, 1999; Kaper et al., 2004). Pathogenic E. coli strains fall into two categories: those that cause intestinal pathologies and those that cause extraintestinal pathologies. Intestinal pathologies mostly consist of more or less severe diarrhoea caused by different East. coli pathotypes such as enterotoxinogenic, enteropathogenic or eastnterohaemorragic E. coli (ETEC, EPEC and EHEC, respectively), potentially evolving into a haemolytic uremic syndrome (HUS) in the case of EHEC infections ( Kaper et al., 2004). Among these pathotypes, EHEC strains of serotype O157:H7 are an established zoonotic pathogen. It is well established that subcontract animals, namely cattle, institute a reservoir of EHEC (O157:H7) ( Manning et al., 2008; Friesema et al., 2010). It is estimated that EHEC causes >75 000 homo infections and 17 outbreaks per yr in North America ( Manning et al., 2008). These infections can evolve into an HUS, leading to death in about 5% of the cases ( Gould et al., 2009).
Extraintestinal pathogenic Due east. coli (ExPEC) are another important group of pathogenic E. coli causing a diversity of infections in both humans and animals including urinary tract infections (UTIs), meningitis and septicaemia. Uropathogenic E. coli (UPEC) are able to colonize the urinary tract and cause cystitis and pyelonephritis, which can lead to urosepsis ( Kaper et al., 2004). An estimated 130–175 million human UTIs occur every year in the earth, with about 80% being acquired by UPEC strains (Russo & Johnson, 2003). ExPEC are also the primary Gram-negative bacterial pathogen associated with neonatal meningitis and the 2d overall cause after grouping B streptococci (Bonacorsi & Bingen, 2005). Gedue northingitis-associated East. coli (MNEC) can cause severe neurological lesions and pb to the death of 20–40% infected newborns (Bonacorsi & Bingen, 2005). ExPEC also constitute i of the chief causes of nosocomial bloodstream infections in nursing homes and hospitals (Ron, 2006). Long-term hospitalized patients tin develop pneumonia, nosocomial bacteraemia or prostatitis (Russo & Johnson, 2003). These infections are even more than difficult to combat when strains are antimicrobial resistant (Ron, 2006). Every bit opposed to intestinal E. coli infections, for which outbreaks are ofttimes reported, ExPEC infections are normally considered equally private or isolated opportunistic infections, even if potentially related infections accept been reported during brusk periods of time in restricted geographical areas (George & Manges, 2010). In contrast to intestinal pathogenic Due east. coli, ExPEC mostly affect a specific subset of the population (newborns, elderly and immuno-compromised patients) or cause UTIs in otherwise salubrious women following faecal contagion of the urogenital tract (Yamamoto, 2007).
Although it is difficult to retrace the origin of ExPEC causing human infections, it is possible that ExPEC from animals could contaminate humans. Indeed, ExPEC are widespread in animate being reservoirs, where they besides crusade diseases. Notably, the poultry manufacture endures severe losses due to colibacillosis caused by avian pathogenic E. coli (APEC). APEC colonize the respiratory tract of poultry and cause airsacculitis, which can develop into septicaemia and generalized infection. APEC outbreaks can lead to up to as much equally 20% mortality in flocks, but also cause losses in product due to decreased growth rate and carcass condemnation at slaughter (Dho-Moulin & Fairbrother, 1999). In cattle, ExPEC are also responsible for UTIs, just more chiefly, are an of import crusade of bovine mastitis. Mastitis is an important economical trouble in dairy cattle and causes decreases in milk production, milk that may exist of unsuitable quality for commercial sale. In some peracute cases, mastitis may even lead to the death of the cows (Fairbrother & Nadeau, 2010). UTIs are likewise an important cause of mortality in developed swine (Fairbrother & Ngeleka, 1994). Moreover, domestic companion animals (dogs and cats) also suffer from infections caused by ExPEC ( Johnson et al., 2008a, b, 2009a, b).
To establish a link betwixt human and animal ExPEC strains, isolates need to exist compared. In the nowadays article, the most contempo work carried out to compare human and animal ExPEC is reviewed. Considering antimicrobial-resistant strains are widespread in brute reservoirs, in part due to the extensive use of antimicrobials, the transmission of ExPEC from animals to humans should exist considered as a potential hazard, fifty-fifty in cases where diseases are likely to be host-specific. Reducing the animal reservoir as a source of ExPEC using measures such every bit vaccines to replace and reduce the use of antimicrobials could reduce losses due to ExPEC in fauna production while limiting the spread of antimicrobial-resistant ExPEC of potential health risk to humans.
Demystifying Due east. coli multifariousness: establishing good criteria to compare isolates
Comparing of E. coli isolates on a large calibration is a considerable challenge because of the wide genetic diversity resulting from genome remodelling and horizontal acquisition from other pathogenic bacteria (Ron, 2010). Such a caste of diversity can brand information technology challenging to determine to what degree specific isolates are related to one another (Manges, 2010). Since the early 1940s, nomenclature by serotype equally defined by Kaufmann (O, Chiliad, H) was used to compare Eastward. coli isolates (Achtman & Pluschke, 1986). In the 1970s, food had already been proposed as a source of contagion of the human abdominal tract by E. coli strains from animal origin ( Bettelheim et al., 1974). An experiment on human volunteers demonstrated that isolates from animal origin could colonize and persist in the homo bowel for long periods ( Cooke et al., 1972). At that fourth dimension, serotypes were used to compare unlike isolates. A written report focusing on strains isolated from meat and from human and animate being faeces showed that in general, amid the typable isolates, no overlap was observed between creature and homo isolates, even if some serotypes associated with UTIs, besides found in the human being faecal flora of healthy individuals, could rarely be plant amidst brute strains ( Bettelheim et al., 1974). Withal, serotypes could not be adamant for all isolates and it has been observed that isolates sharing the same serotype tin can be genetically distinct ( Achtman et al., 1986). Consequently, O:K serotyping solitary is not appropriate to compare Eastward. coli isolates.
Progressively, other criteria such every bit migration of the outer membrane poly peptide profiles, plasmid contents or virulence-associated characteristics (haemolysin production, haemagglutination, production of fimbrial adhesins and other phenotypes) were added to compare human and creature isolates ( Achtman et al., 1983, 1986; Achtman & Pluschke, 1986). Information technology appeared that clonal groups did not always correlate with serogroups, but rather with the presence of specific virulence factors. Thus, the presence or absence of specific virulence factors was adopted and has get an important means of classifying E. coli isolates, and recent studies often apply these criteria in add-on to serotyping and newer molecular methodologies ( Wang et al., 2010).
Multiplex PCR analysis is used to make up one's mind the prevalence of virulence-associated genes within ExPEC (Johnson & Stell, 2000). Table i presents the genes used normally for virulence genotyping. Genes related to iron-siderophore production and uptake, bacterial adhesion, toxin production, protectins and a few others are the about widely used to constitute the ExPEC genotype. Some virulence factors are mutual to animal and man ExPEC. Factors involved in iron acquisition have a loftier prevalence in ExPEC isolates. In avian and mammalian tissues and claret, iron is bound to proteins such every bit transferrins and iron-chelating systems are cardinal virulence factors required to scavenge iron from these host proteins (Ron, 2010). Adhesins mediate specific bounden to host receptors. ExPEC produce a wide variety of adhesins, which might help them adapt to different host tissues ( Antao et al., 2009). However, the expression of some adhesins is not specific to ExPEC. Type I fimbriae are produced past over 95% of E. coli isolates. These fimbriae enable the transitory colonization of the oropharyngeal tract and allow faecal/oral transmission betwixt hosts ( Sokurenko et al., 1998). Although FimH (mannose-binding adhesion of the type I fimbriae) plays a cardinal function in UTIs ( Chen et al., 2009), fimH is establish in other ExPEC strains. In APEC, the expression of type one fimbriae is prominent in the upper respiratory tract, whereas phase variation to the nonfimbriated grade may be favoured in the lower respiratory tract to reduce uptake and killing by phagocytes ( Pourbakhsh et al., 1997; Mellata et al., 2003). The presence or absence of fimH is bereft to determine the virulence potential of the strains, as naturally occurring variants presenting dissimilar bounden properties have been described, some beingness more prevalent in UPEC, while others are mostly represented among intestinal isolates ( Sokurenko et al., 1998). Genes coding for toxins are represented in ExPEC and are therefore often used to categorize ExPEC isolates. If toxins practice not seem to play a disquisitional office in the virulence of septicaemic E. coli ( Mokady et al., 2005), α-haemolysin (HlyA) and cytotoxic necrotizing cistron 1 may play a role in the virulence of UPEC ( Wiles et al., 2008). Virulence factors associated with E. coli causing extraintestinal infections are non also defined as those involved in intestinal infections, equally strains having very unlike combinations of virulence factors can cause similar pathologies. For example, very few virulence factors are mutual among Due east. coli strains isolated from cases of septicaemia and it is likely that different strains harbour a variety of distinct virulence factors that can provide similar roles at different stages of the infection process (Ron, 2010). Genotyping of ExPEC virulence-associated traits helps define and compare strains, simply it is non e'er a good indicator of virulence potential.
Table i
ExPEC virulence-associated genes present in human being and/or animal isolates and their boilerplate percent of prevalence in clinical isolates.
Table one
ExPEC virulence-associated genes present in man and/or brute isolates and their average percentage of prevalence in clinical isolates.
Over the final decade, the implementation of molecular biology and technological advances has provided improved methods to compare strains, with the near recent existence the complete genome sequencing of strains ( Moriel et al., 2010). As complete genome sequencing is not yet a applied option for comparing a large number of isolates, most recent studies utilise a combination of phylogenetic typing ( Clermont et al., 2000), multilocus sequence typing ( Wirth et al., 2006), pulsed-field gel electrophoresis typing ( Ribot et al., 2006), plasmid assay and diagnostic DNA microarrays ( Hamelin et al., 2006).
Animals constitute a potential reservoir for contagion of humans by ExPEC
ExPEC strains are associated with infections in a multifariousness of animals, but are particularly mutual in both humans and poultry (Russo & Johnson, 2003; Lutful Kabir, 2010). These pathogens are isolated from livestock (poultry, cattle, swine), pet animals (dogs, cats, horses) and wildlife (brown rats and birds) ( Achtman et al., 1986; Schierack et al., 2008; Johnson et al., 2009a, Ewers et al., 2010; Guenther et al., 2010a, b; Sheldon et al., 2010). Reports presenting similarities among the diverse ExPEC strains, the common phylogenetic origins of strains isolated from humans and animals, besides as their genome flexibility raise concerns about the potential for ExPEC to cause zoonosis ( Johnson et al., 2007b; Brzuszkiewicz et al., 2009). In every bit much every bit intestinal human microorganisms contains potential ExPEC strains, it is also plausible that animals are a reservoir of ExPEC that have the potential to cause human diseases, as has been shown for sure East. coli infections (Fairbrother & Nadeau, 2006).
UPEC colonize the intestine before causing an ascending UTI (Yamamoto, 2007). The faecal flora of humans and animals are considered a reservoir of UPEC ( Yamamoto et al., 1997; Johnson et al., 2003a). UPEC isolated from dogs, cats and humans are in some cases phylogenetically closely related ( Johnson et al., 2001, 2008b). Moreover, such strains can cross the species bulwark and effectively colonize humans too as companion animals such as dogs and cats ( Johnson et al., 2009b). Cats and a canis familiaris within a household were found to exist colonized past the aforementioned UPEC strain ( Johnson et al., 2009b). A UPEC strain that caused UTI in a dog besides colonized 4 humans in the aforementioned residence. A previous UTI episode in the same household caused by a different UPEC strain infecting the homo mother was likewise plant colonizing three human being family members and the dog ( Johnson et al., 2008a). These reports introduce evidence not only for human-to-homo transmission only also for animate being-to-human and human-to-beast transmission of ExPEC. Dogs and cats should therefore be considered as potential reservoirs for the manual of UPEC to humans. Regardless of whether the strains may be host-specific or non in their ability to cause a disease, there is a take a chance of contamination and persistence of homo UPEC in the intestinal flora of companion animals.
Another reservoir of ExPEC with zoonotic potential is constitute in poultry. APEC cause a systemic infection by first infecting the respiratory tract and then disseminating to organs. Although the intestinal tract of poultry is not recognized as the direct route of entry for APEC, it is a probable reservoir of APEC strains. Certain colibacillosis outbreak and non-outbreak strains isolated from avian intestinal organs, faeces and environment are highly similar to human ExPEC ( Johnson et al., 2007b; Ewers et al., 2009; Mora et al., 2009, 2010).
Some virulence traits are more than prevalent in specific groups of homo or animal ExPEC strains, suggesting that certain virulence genes or ExPEC pathotypes may be associated with humans or specific animal species ( Rodriguez-Siek et al., 2005; Ewers et al., 2007). Notwithstanding, in many cases, the identification of mutual virulence factors and in vivo or in vitro virulence assays do not correlate with host specificity. For example, contempo studies have demonstrated that some ExPEC strains are virulent or capable of infecting both poultry and mammals (Tabular array 2), farther supporting the zoonotic potential of certain APEC strains. As more isolates are analysed and molecular genetic techniques are applied to farther define E. coli clonal groups, the ambivalence about whether ExPEC infections are host specific or of zoonotic potential will likely remain because the diversity of ExPEC strains supports arguments for either of these hypotheses (Ron, 2006). Despite this, at that place is mounting evidence that certain ExPEC clonal groups are capable of causing both human and animal infections.
Tabular array ii
ExPEC strains able to infect both mammals and poultry
Tabular array 2
ExPEC strains able to infect both mammals and poultry
While the transmission of a faecal E. coli strain from chickens to farm workers has been documented ( Levy et al., 1976), widespread broadcasting of ExPEC strains from poultry reservoirs to humans through food contagion is of far greater concern. ExPEC isolated from sick chickens and humans exercise not always correspond genetically ( Caya et al., 1999), but in many recent studies, profiles of strains isolated from retail meat resembled, and in some cases matched, those of human ExPEC clinical isolates ( Johnson et al., 2003b, 2005a, b; Santo et al., 2007; Jakobsen et al., 2010; Vincent et al., 2010). These findings reinforce the hypothesis that some human ExPEC diseases could arise from poultry and pig ExPEC reservoirs post-obit contamination of the meat in slaughterhouses or in retail-nutrient markets. Although it may be difficult to rule out whether or not the presence of ExPEC on meats or other foods may be due to contamination from man sources during processing, there are cases where ExPEC populations found on retail meat are closely related to ExPEC isolated from food animals ( Jakobsen et al., 2010).
In addition to causing colibacillosis in poultry and man infections, ExPEC are also an important crusade of bovine mastitis. The adventure of manual of ExPEC from bovine to humans through milk consumption could be minimized, because that in most developed countries, measures exist to avert bacterial contamination of milk and raw milk consumption is often banned. Moreover, to our knowledge, no evidence has been establish to associate strains causing bovine mastitis to human diseases.
ExPEC could be transmitted from poultry to humans through meat consumption, merely another plausible route of transmission from animal reservoirs to humans is via environmental contamination from manure or faeces of wild or domestic birds ( Duriez et al., 2008; Graham et al., 2008; Guenther et al., 2010b). Isolates corresponding to ExPEC pathotypes were institute in aquatic ecosystems ( Hamelin et al., 2007). Therefore, it is possible that contamination of fruits and vegetables ( Vincent et al., 2010) occurred in fields or maybe later on during nutrient processing. Cantankerous-contamination between meat products and other foods prepared on the same ecology surfaces or with the aforementioned utensils is besides possible. Transmission of ExPEC to humans who do not eat meat products might then occur via environmental contamination. Whether or not ExPEC transmission from animate being reservoirs to humans may occur through nutrient, ecology or h2o contamination is still unclear as epidemiological testify is lacking. For about outbreak and non-outbreak community-acquired infections acquired by ExPEC, the source of the strain is unknown (George & Manges, 2010). There is an important lag in agreement how ExPEC disseminate maybe because of their diversity in multiple hosts.
Whenever ExPEC outbreaks occur in humans and animals, investigations using the latest typing techniques should be performed to determine the potential source of the outbreak. Molecular epidemiology studies involving human, animal, nutrient and ecology isolates are needed to gather more evidence about the zoonotic potential of ExPEC and to appraise all risks of animal reservoirs to human health. One of the well-documented risks associated with transmission of ExPEC from animate being reservoirs, in improver to the spread of potential disease, is the dissemination of resistance to antimicrobials.
Emergence and transfer of antimicrobial resistance
Antimicrobials take been widely used in animal husbandry to prevent disease, reduce infections and promote animal growth. Antimicrobial usage as growth promoters is no longer permitted in the European Matrimony, but is still currently practiced in other parts of the world ( Bonnet et al., 2009). The utilize of antimicrobials has resulted in pick for antimicrobial-resistant E. coli in the commensal microbiota that could contaminate humans through consumption of contaminated meat ( Aarestrup et al., 2001). Studies of broiler chickens accept reported a loftier charge per unit of antimicrobial multiresistant E. coli ( Diarra et al., 2007). In spite of the ban on antimicrobials applied in Europe, antibiotic-resistant strains are persistent in broiler houses ( Heuer et al., 2002). The use of antimicrobials does not lead to the selection of virulent strains ( Johnson et al., 2004), but rather to the spread of resistance genes among commensal strains. In a recent study, virulence plasmids and multidrug resistance plasmids were not establish in the same strains ( Bonnet et al., 2009). On the other mitt, hybrid resistance plasmids encoding both multiple resistance to antimicrobials and virulence-associated genes were found in some APEC strains, and these strains were able to infect human cells and cause meningitis in rats ( Johnson et al., 2010).
The fact that antimicrobial resistance genes are establish on mobile genetics elements enables their rapid spread among the bacterial population ( Guardabassi et al., 2004). In homo medicine, UTIs due to ExPEC were traditionally treated with ampicillin or trimethoprim sulfamethoxazole (TMP-STX). ExPEC resistance to these agents as well equally to extended-spectrum β-lactamases, aminoglycosides, tetracyclines and fluoroquinolones is at present frequently observed ( Maslow et al., 2004; Smith et al., 2007; Wieser et al., 2010). Resistance to antimicrobial agents could lead to an increase in mortality also as a longer elapsing of treatments and hospitalizations, as has been observed for other pathogens (Molbak, 2004). Manual of ExPEC strains resistant to streptothricin and apramycin from subcontract animals to farm workers and their families has been reported ( Maynard et al., 2004; Molbak, 2004). Studies have likewise shown the presence of antimicrobial-resistant ExPEC in farm animals and in meat products ( Maynard et al., 2004; Johnson et al., 2005a, b, 2007a; Zhao et al., 2005; Kim et al., 2007; Jakobsen et al., 2010). In recent years, at that place have been accumulating information that support the likelihood that animal reservoirs could be responsible for contamination of humans with antimicrobial-resistant ExPEC and other bacteria through the consumption of contaminated food ( Johnson et al., 2005b, 2007a; Hannah et al., 2009). Recently, in the United States, the advent of related UPEC resistant to TMP-STX causing human UTI cases during the same period suggests a foodborne contamination from animal products ( Ramchandani et al., 2005). In addition, even though no existent data on antimicrobial use for small animals in veterinary medicine are available, it appears that the effect of contact with domestic cats and dogs to spread antimicrobial resistances has been underestimated ( Guardabassi et al., 2004). In some cases, the same classes of antimicrobials are used in human and veterinary medicine and indeed cases of ExPEC transmission from pet animals to humans have been reported ( Johnson et al., 2008a). Antimicrobial-resistant ExPEC could also spread in the surroundings from subcontract wastes. Indeed, an E. coli strain carrying both APEC-type virulence plasmid and multidrug resistance has been isolated from an industrially polluted surround ( Fricke et al., 2008).
The utilise of antimicrobials in agriculture, subcontract management and in veterinary medicine including livestock and companion animals favours dissemination of antimicrobial resistance in animal reservoirs and the environment, leading to increased resistance to antimicrobials in bacteria colonizing humans. The inappropriate utilise of antimicrobials in man medicine too plays an important role in this complex problem. Every bit such, antimicrobial use should exist reduced to a minimum and alternative approaches should exist used to limit the spread of antimicrobial resistance in animals and humans.
Conclusion
The employ of molecular techniques over the last decade has helped get together mounting show that animals could constitute a reservoir of ExPEC, thus presenting a potential threat to human health. Animal reservoirs of ExPEC could cause diseases, but likewise spread antimicrobial resistance, therefore increasing the risk of incidence of human infections and complicating their treatment. Being aware of these risks should help put in identify measures to reduce the take chances of food and water contamination by ExPEC, only too to limit the use of antimicrobials in animals. Ane possible solution to limit the presence of ExPEC among either animals or humans is the use of vaccines made of broadly conserved ExPEC antigens (Dobrindt & Hacker, 2008; Alteri et al., 2009; Moriel et al., 2010; Wieser et al., 2010). The use of vaccines for animals and humans should decrease the number of infections and reduce the demand for antimicrobial use. Equally a effect, information technology should reduce the selection pressure for resistant strains and potentially reduce the take a chance of homo contamination past antimicrobial-resistant ExPEC.
Authors' contribution
L.B. and A.Thou contributed equally to this work.
Acknowledgements
This work was supported by grants from Ministère de l'Agriculture, des Pêcheries et de l'Alimentation du Québec (MAPAQ) and in function from the Natural Sciences and Technology Research Council of Canada (NSERC) to C.M.D. and J.H., NSERC Industrial R&D Fellowship to L.B. and the Fondation Armand Frappier-Postdoctoral Fellowship to A.1000.
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Author notes
Editor: Eric Oswald
© 2011 Federation of European Microbiological Societies.
Source: https://academic.oup.com/femspd/article/62/1/1/519216
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