Mechanisms of Pathogenic Escherichia coli Attachment to Meat

Abstract

Escherichia coli are present in the human and animal microbiome as facultative anaerobes and are viewed as an integral part of the whole gastrointestinal environment. In certain circumstances, some species can also become opportunistic pathogens responsible for severe infections in humans. These infections are caused by the enterotoxinogenic E. coli, enteroinvasive E. coli, enteropathogenic E. coli and the enterohemorrhagic E. coli species, frequently present in food products and on food matrices. Severe human infections can be caused by consumption of meat contaminated upon exposure to animal feces, and as such, farm animals are considered to be a natural reservoir. The mechanisms by which these four major species of E. coli adhere and persist in meat postslaughter are of major interest to public health and food processors given their frequent involvement in foodborne outbreaks. This review aims to structure and provide an update on the mechanistic roles of environmental factors, curli, type I and type IV pili on E. coli adherence/interaction with meat postslaughter. Furthermore, we emphasize on the importance of bacterial surface structures, which can be used in designing interventions to enhance food safety and protect public health by reducing the burden of foodborne illnesses.

Introduction

The pathogenic serotypes of Escherichia coli are responsible for infections in humans and animals (Le Bouguénec, 2005). Since its discovery, over 160 years ago, by Theodor Escherich in infant feces, E. coli has been extensively studied not only for its role as a participant in the structure of the animal and human microbiome but also for the significant health impact in the infected hosts by the pathogenic strains (Hacker and Blum-Oehler, 2007). Contamination of raw meat by E. coli has always been an important issue for food safety and retailers take measures to limit meat contamination. E. coli are nonsporing rod bacteria, part of the family Enterobacteriaceae and of the genus Escherichia, are characterized as being catalase positive, oxidase negative, and fermentative Gram negatives (Lim et al., 2010).

E. coli growth conditions include temperatures from 7°C to 50°C (37°C optimum); however, some enterotoxinogenic E. coli (ETEC) strains can grow at temperatures as low as 4°C (Tuttle et al., 2021). The family Enterobacteriaceae, part of the order Enterobacterales is causing ∼265,000 illnesses and 100 deaths per year in the United States (Jnani and Ray, 2024), emerging as one of the most important human pathogens globally (Poolman et al., 2023). The members of this family are unicellular organisms expressing type I fimbriae, type IV fimbriae, and curli on the bacterial surface involved in attachment and biofilm production (Puri et al., 2023).

Another member of this genus is represented by the enteroinvasive E. coli (EIEC), which is known for causing infections leading to severe diarrheal diseases, similar to Shigella, upon invasion of epithelial cells in humans (Diez-Gonzalez et al., 2024). The PCR identification of EIEC would include the amplification of the ipaH gene, biochemical and serological assays using antisera to differentiate EIEC from noninvasive E. coli as well as Shigella (Lampel, 2014). Human infections are generally caused by the consumption of contaminated read-to-eat foods as described in an outbreak in Denmark caused by contaminated fresh vegetables (Torpdahl et al., 2023).

Enteropathogenic E. coli (EPEC) was first described in the 1940s in an outbreak of infant diarrhea in the United Kingdom; however, they are highly prevalent in developing countries (Kaper et al., 2004). It has been highlighted that food animals are reservoirs of virulent EPEC isolates with implications for food safety and zoonotic infections and it is essential that they are monitored through one health strategy (Milton et al., 2023). They are prevalent in young livestock, as highlighted in a study investigating EPEC presence in 0- to 4-month-old lambs with (n = 230) and without diarrhea (n = 108) from a Sheep Research Station in India. EPEC were isolated from both lamb with (6.1%) and of lambs without (11.1%) diarrhea and constituted the first report of EPEC in lambs, emphasizing its adaptability in various hosts (Wani et al., 2009).

The one health approach in this instance is strategically beneficial as it has been shown that they are also highly prevalent in domestic pet animals (cats) helping in designing a strategy to control multidrug-resistant E. coli infections (Das et al., 2023). Enterohemorrhagic E. coli (EHEC), known as verotoxin-producing E. coli (VTEC), also known as Shiga toxin–producing E. coli (STECs) are commonly found in outbreaks associated with severe clinical illness (Bugarel et al., 2011). Human infections are generally known as hemorrhagic colitis and hemolytic uremic syndrome and are associated with the consumption of contaminated foods (Tzschoppe et al., 2012).

Livestock carcasses are usually contaminated by feces, and are responsible for the spread of EHEC via contaminated meat to humans (Elder et al., 2000). To reduce the spread of bovine EHEC, on-farm interventions are necessary and progress has been made via diet-based strategies to reduce the prevalence of E. coli in bovines preslaughter (Callaway et al., 2003). The diet-based strategy showed that eliminating abruptly a high grain diet to a forage diet the generic E. coli was reduced 1000-fold within only 5 days, with these bacteria being less able to survive the acid shock in the human stomach.

Bacterial adhesion to animal tissues has been extensively reviewed overall, but not from a food safety point of view, and was shown to involve the recognition of host extracellular matrix (ECM) components (collagen, fibronectin, laminin, and elastin) (Chagnot et al., 2012). Much is known about the interaction of E. coli with cell structures during infection and disease; however, the information related to the mechanisms of meat matrices colonization has been poorly discussed so far. In this review we aimed to focus on the E. coli surface organelles (curli, type I and IV fimbriae) and on their mechanisms of adhesion to livestock meat from a food safety perspective postslaughter and based on survey data.

Factors Mediating Bacterial Attachment to Meat

Temperature, pH, osmolarity, nutrient availability, and the local microbiota play an important role in the process of bacterial attachment to meat (Giaouris et al., 2005). In addition to these factors, bacterial concentration, the type of meat and the bacterial strain are also enabling factors affecting the bacterial attachment. E. coli attachment to the ECM, including collagen I, collagen IV laminin, and fibronectin, apparently is not effected by pH (5–9); however, the impact of salt type and concentration (0.1–0.85% of NaCl, KCl, and 10% of CaCl₂) was variable and strain dependent (Zulfakar et al., 2013). Later, in this review we discuss the interaction between bacterial surface structures and the ECM structures fibronectin and laminin. Although it is no longer a current practice in slaughtering facilities, evidence suggests that, beside salinity and pH, electrical charge is also involved in the attachment process of bacteria to meat surfaces, with some reduction in bacterial attachment being observed in electrically stimulated meat (Dickson and Crouse, 1989). The ability of pathogenic E. coli to upregulate genes for glycine betaine osmoprotectant uptake is precisely designed to support the bacterium growth at low pH (3.5), justifying the lack of impact against bacterial attachment to ECM in such conditions (Bergholz et al., 2009). Moreover, the ability of other foodborne pathogens (e.g., Salmonella enterica) to attach to the ECM in a pH variable meat processing environment could also be enhanced by their fat content (Waterman and Small, 1998).

The rate of bacterial attachment and survival on food matrices is influenced by the cell surface organelles and the food surface attraction mediators, including pH, temperature, and the food structure itself (Tan et al., 2014). The attachment to biotic or abiotic surfaces is mediated by these surface structures and includes fimbriae, pili, curli, and flagella (Austin et al., 1998). Osmolarity has a significant effect on biofilm formation (Leech et al., 2020) by directly regulating curli production (Jubelin et al., 2005) in E. coli. It has been shown that curli presence is indeed associated with increased cell hydrophobicity and E. coli O157:H7 attachment to food surface (Boyer et al., 2007). In E. coli, the bacterial surface plays a significant role in bacterial adherence to the food surface owing to the hydrophobicity of the outer surface (Ukuku and Fett, 2002). These hydrophobic properties will ensure attachment to meat skin, muscle, or to the fat layers, and enhances their survival rate in such conditions (Selgas et al., 1993).

The growth rate of generic E. coli, at 10°C, and E. coli O157 and non-O157 in raw pork is significantly different and dependent on the fat content (5% vs. 25%). The fat content had a significant effect on the generic E. coli, E. coli O157, and non-O157 growth, suggesting its potential biomarker role in meat processing facilities (Haque et al., 2023). Temperature will also affect adherence by directly impacting of bacterial attachment to meat surface primarily because it affects the growth and morphology of bacteria (Kumar and Libchaber, 2013). In E. coli O157:H7 temperature affects formation of curli and biofilm, at low temperatures (4°C), suggesting the relevance of temperature control in meat processing facilities (Carter et al., 2016).

Environmental and animal E. coli isolates are also affected by fluctuations in temperature (37°C and 20°C), which regulates the genetic switch (fimS) that controls phase variation in these bacteria (Marshall et al., 2016). Temperature regulation of type IV fimbriae production was described initially in Legionella pneumophila (Liles et al., 1998) and later in E. coli (Hinthong et al., 2015).

Oxygen availability controls regulatory mechanisms of fim expression and contributes to the formation of the ECM components and subsequently to the biofilm structure by influencing fimbriae formation (Floyd et al., 2015). Bacterial contamination of meat is impacted by oxygen starvation affecting their growth, motility, chemotaxis, and reduces meat penetration (Shirai et al., 2017). Nevertheless, regardless of the oxygen concentration toxin expression in pathogenic E. coli is not affected (James and Keevil, 1999). Under oxygen limitation the persistence of fimbria and the maintained ability to express toxins explains partially their ability to cause disease in the oxygen-limited conditions of the urinary tract (Lane et al., 2009).

Role of Bacterial Curli

Curli play a central role in cell-to-cell interaction (Prigent-Combaret et al., 2000) and attachment to food matrices (Boyer et al., 2007). First discovered in the 1980s, in bovine mastitis samples, curli are E. coli surface organelles formed of curlin protein subunits encoded by the csgA gene (Barnhart and Chapman, 2006). When csgA is inactivated an 80% reduction in bacterial adhesion is observed (La Ragione et al., 2000). As surface adhesive structures, they are essentially involved in bacterial biofilm formation on organic surfaces (Visvalingam et al., 2019). It has been shown that E. coli EHEC strains that do not produce curli are not only less motile but also less able to produce biofilm, hence their importance in pathogen persistence in meat processing environments (Lajhar et al., 2018).

However, E. coli persistence in meat processing environments is not always dependent on their ability to form biofilm, although the ability to produce curli is present in most meat isolates from such environment (Yang et al., 2023). Moreover, E. coli meat isolates, described as curli producing strains and differentiated by the presence of the csgA gene, are highly pathogenic (Barilli et al., 2020). It is apparent that these highly pathogenic strains (e.g., EHEC) and specifically those isolated from beef carcasses, in their majority, have the ability to express curli, whether those isolated from abiotic surfaces express curli almost exclusively (Stanford et al., 2021). First, the specific requirement for curli presence to attach to abiotic surfaces is probably explained by the extra strength needed to attach and form biofilm on such surfaces.

Second, the attachment to biotic surfaces is linked to curli presence, because curli-expressing bacterial cells (EHEC) have a closer association with organic surfaces (beef) compared with noncurli-expressing EHEC cells (Chen et al., 2007). The ability to form biofilms and produce curli by E. coli isolates does not appear to be correlated with their ability to survive in a specific environment. For example, it has been shown that most soil-persistent E. coli isolates are curli positive; however, these are not required for long-term survival in soil (Somorin et al., 2018). However, in the animal gastrointestinal tract, the presence of curli will allow E. coli O157:H7 to sustain a longer colonization period in cattle (Sheng et al., 2020). It is evident that regardless of their origin, pathogenic E. coli expressing curli have the potential to form strong biofilms and become a risk to food safety in meat processing environments.

Like type I fimbriae, the ability to express curli and increased antimicrobial resistance (AMR) are traits that will provide the E. coli isolates with an increased aptitude to persist in the production chain (Projahn et al., 2018). This is particularly important in disease as it has been shown that E. coli is able to produce curli in both aerobic and anaerobic conditions indicating that eradication of multidrug-resistant (MDR) E. coli in these environments will be difficult (Karczmarczyk et al., 2008). It is also apparent that curli-producing E. coli O157:H7 are less resistant to acid stress compared with their curli-deficient counterparts; however, the decrease in resistance was attributed to the Rcs CDB two component signal transduction system that decreases curli production and increases acid resistance in hamburger-associated outbreak strains (Carter et al., 2012).

There is also significant evidence to suggest that E. coli O157:H7 outbreak isolates, linked to the consumption of hamburgers, steak, beef, and other food products lack curli expression, suggesting that curli-deficient phenotypes are a selective trait for survival of E. coli O157 in agricultural environments (Ravva et al., 2016). As discussed in this section, once these isolates passage through the gastrointestinal environment, the E. coli curli expression is reversed switching from sedentary to the motile-adhesive phenotype (Pesavento et al., 2008). This close relationship between curli production and environmental conditions also relates to curlin production and its expression by the csgA gene.

The expression of csgA by E. coli O157:H7 significantly affected the bacterium ability to attach to abiotic surfaces (glass, Teflon, and stainless steel) suggesting altered behavior in various environments (Goulter-Thorsen et al., 2011). This csgA-dependent increase in the bacterium ability to attach and form biofilm has been described in chicken meat isolates, in a Turkish study (88.5% of all isolates), and was potentially caused by cross-contamination during processing (Dishan et al., 2023). This trend was further confirmed in an Indian study, where the authors have identified that 91.48% of the avian pathogenic E. coli (APEC) isolates were positive for the csgA gene suggesting its relevance to biofilm formation in poultry farms (Grakh et al., 2022). Of interest, these types of isolates, also related to colibacillosis cases, one of the most common diseases in poultry (Lozica et al., 2021), suggesting their involvement in disease development.

The direct relationship between curli formation and food safety was established in a study that aimed to recover E. coli EHEC from processed ready-to-eat (RTE) meats (Beshiru et al., 2022). They were found to mediate E. coli binding to the fibronectin molecules of meat (Arnqvist et al., 1992) and promote bacterial internalization into the host cells (Gophna et al., 2001). The percentage of EHEC expressing curli, isolated from RTE meats was 62.9% and was significantly correlated with cellulose formation (p < 0.01). The importance of curli formation over cellulose in the attachment of E. coli O157:H7 was proven in earlier study indicating that curli fibers are essential for surface attachment, whereas cellulose was dispensable (Macarisin et al., 2012). Consequently, blocking bacterial attachment and biofilm formation could be included as a strategy to design anti-curli interventions. This approach is strengthened in a study showing that caffeine could inhibit E. coli biofilm formation through the regulation of curli biogenesis and significantly reduce biofilm formation (85–91%) (Rathi et al., 2022).

Role of Type I Fimbriae (Pili)

Known for their role in bacterial attachment to epithelial cells, type I fimbriae contribute significantly to host colonization (Vila et al., 2016). They are indeed the adhesion organelles contributing to bacterial attachment to inflammatory cells in vitro; however, much more must be done to fully understand its virulence implications (Connell et al., 1996). Most of the existing literature links their expression in E. coli to urinary tract infections (UTIs), expression that is dependent on phase variation in vivo (Struve and Krogfelt, 1999). However, their role in human disease is not directly linked to mucosal inflammatory response in human UTIs (Bergsten et al., 2007).

Upon cell internalization they contribute to bacterial survival and antibiotic evasion and are even of considerable importance in the context of major infections (Avalos Vizcarra et al., 2016). These uropathogenic E. coli (UPEC) isolates are genetically related to meat isolates (poultry, beef, pork) (Garcia et al., 2023). These animal-derived isolates were shown to carry the type I fimbriae operon alongside other virulence-related genes suggesting that food production animals are a major source of UPEC. Type I pili (fimbriae) act as virulence factors and are used by E. coli to attach and invade epithelial cells (Wolf and Arkin, 2002). Their expression is phase variable and is controlled by site-specific DNA inversion of the fim operon (Sohanpal et al., 2001). The activity of this fim operon is increased following host interaction, hence their role in pathogenesis (Sheikh et al., 2017).

Pathogenic E. coli meat isolates (STEC) are often expressing type I pili as described in isolates originating from Malaysian beef (Wameadesa et al., 2017) and in Thailand (Sukkua et al., 2017). Their detection in STEC is also correlated with increased adherence to abiotic surfaces enhancing their survival in such environments (Cookson et al., 2002). Type I pili also mediate E. coli attachment to the host epithelium via the mannose subunits of the glycoproteins on the surface of the urinary epithelium (Capitani et al., 2006). This is not the case for all E. coli strains, including VTEC isolated from cattle and humans, suggesting that type I pili can be considered as candidate target for diagnostic (Enami et al., 1999).

Type I fimbriae are chromosomally encoded by the fim gene cluster and are arranged in a tight right-handed helical rod (Brinton, 1965). Structurally, it is formed by the FimF, FimG, and FimH pilus proteins (Jones et al., 1995; Krogfelt et al., 1990) and the FimC and FimD chaperone proteins; however, those are not part of the final structure (Jones et al., 1993; Orndorff and Falkow, 1984). FimH has two domains, the mannose-binding lectin and the fimbria-incorporating pilin, which are connected through a linker. At the mannose-binding lectin end it has a β-barrel–shaped mannose binding pocket strongly linked to UTIs (Foroogh et al., 2021). They are considered adhesive protein-like structures involved not only in virulence, but also in the adherence and biofilm formation (Day et al., 2021).

Accordingly, it has been suggested that UTI FimH variants of E. coli are more likely to form biofilms specifically to medical implants and catheters (Schembri and Klemm, 2001). One of the most prevalent extraintestinal pathogenic E. coli is the ST131 clone that was previously associated to retail meats (Bergeron et al., 2012; Kluytmans et al., 2013). In a study examining the prevalence of sequence type 131 (ST131) among meat isolates and clinical isolates, it was concluded that 15.3% of the clinical isolates belonged to ST131 and only 1.3% of the meat isolates (25) were also categorized under the ST131. However, the same study showed that 96% of the meat isolates (24/25) corresponded to the four major fimH alleles of ST131 and only 13% of the human clinical isolates were fimH typed (Liu et al., 2018).

A later study linked antibiotic resistance to E. coli fimH type (broiler origin) indicating a direct relationship between virulence and antibiotic resistance as a bacterial screening objective (Roer et al., 2019). Indirectly these data demonstrate that fimH can be detected among E. coli meat isolates and suggests its association with increased AMR and enhanced virulence potential.

There is increased evidence that a high prevalence of type I fimbriae E. coli in meat matrices is also connected to MDR and boosted ability to form biofilm (Barilli et al., 2020). This statement is supported in a study highlighting that ampicillin, fluoroquinolones, tetracycline, sulfonamides, and colistin-resistant chicken isolates express this phenotype. These resistant chicken isolated clones (ST410 and ST471) were transferred from chicken to households, and all shared the fimH virulence genes (Benlabidi et al., 2023). Similar results were observed in APEC strains associated with colibacillosis worldwide. Specifically, of 392 APEC isolates, 130 were of farm origin and proven to harbor fimH in a proportion of 75–100% and also to express increased resistance to antibiotics (Saha et al., 2020).

The association between virulence and fimH subtype (ST) was also made between food isolates and interconnected by the presence of stx1, stx2, eacA, and hlyA virulence genes in serogroups O26:H11, O91:H21, O111:H2, and O103:H2. This association was emphasized in a study identifying that the fimH gene was detected in 75% of E. coli (ETEC) isolated from Egyptian cheese (Hussien et al., 2019). Moreover, the information presented previously associates MDR with increase in virulence in pathogenic E. coli isolates. If MDR and fimH ST are correlated, then biofilm formation in food production premises can pose a significant threat to the consumer's health. Still, it is evident that the association between MDR E. coli, virulence, and fimH is not only specific to food isolates. Ruminants, for example, as hosts of pathogenic E. coli (Shridhar et al., 2019) can also carry highly virulent MDR fimH isolates originating from wild birds (Ibrahim et al., 2023).

The assumption that in pathogenic E. coli there is always a connection between type I fimbriae, virulence genes, and AMR, does not apply in all instances. Such a case has been made for E. coli isolates resistant to an extended spectrum of cephalosporins (ESC), originating from retail chickens (Buberg et al., 2021). All 141 ESC isolates exhibited uropathogenic-associated virulence factors, including type I fimbriae; nevertheless, there was sufficient significant variability between isolates to suggest that ESC-resistant E. coli from chicken meat can also have low uropathogenic potential in humans.

Fimbria type adhesins are often associated with increased mortality in farmed animals, especially in chicks posthatching owing to infectious omphalitis (Brandly, 1932). A study, investigating the prevalence of fimH genes in omphalitis E. coli isolates, indicated that 77.8% of the isolates were positive for fimH (Ghanbarpour and Salehi, 2010). The involvement of fimH in E. coli adhesion to avian trachea has been efficiently inhibited by monoclonal antibodies 7C2 and 7D8 (Chen et al., 2023), suggesting that this approach could be successfully implemented to prevent contamination of meat and eggs during the industrial production cycles. There is no direct evidence that fimH is involved in E. coli adherence to eggshell surface. However, fimC has been shown that its inhibition by natural antimicrobials will significantly reduce E. coli ability to colonize the eggshell (Corcionivoschi et al., 2023). The same study shows that the attachment to poultry skin and straw bedding was also inhibited.

Biofilms formed on meat products are usually stronger when multiple pathogens are involved in biofilm assembly (Liu et al., 2023). Type I fimbriae are involved in the formation of such biofilms when E. coli and Pseudomonas fragi are in coculture. In these type of biofilms they upregulate the expression of type I fimbriae gene complex and of a dual phosphate response regulator with significant impact on food biocontrol (Haddad et al., 2009; Zhang et al., 2023). This expression pattern of type I fimbriae during biofilm formation was specifically described in STEC as a consequence of interaction with biotic and abiotic surfaces (Matheus-Guimaraes et al., 2014).

Role of Type IV Pili

Type IV pili (polar) are known for their role in bacterial adhesion to host epithelial cells and for their critical role in disease (Miller et al., 2006) owing to their presence in both Gram-negative and Gram-positive bacteria (Melville and Craig, 2013). Type IV pili, located on the bacterial surface, are filamentous structures of major importance in E. coli virulence (Karami et al., 2021), twitching motility, DNA uptake, and in microcolony formation (Craig et al., 2019). Structurally they are composed of proteins called pilins (Jacobsen et al., 2020) creating a highly flexible structure involved in bacterial adhesion, motility, and biofilm formation (Piepenbrink and Sundberg, 2016). They also promote bacterial invasion of epithelial cells and the specific binding to the host laminin and fibronectin located in the host ECM (Xicohtencatl-Cortes et al., 2009).

The importance of ECM during E. coli EHEC colonization of meat highlights the importance of muscle type in bacterial adherence, rather than the specific myofibers (Chagnot et al., 2017). Adherence to the skeletal muscle at the ECM is also mediated by the pili alongside other colonization factors (Chagnot et al., 2013; Chagnot et al., 2012). The bacterial attachment is primarily located at the collagen fibers as shown by scanning electron photomicrographs (Fratamico et al., 1996). The attachment to bovine tissues has indeed been confirmed via the collagen fibrils (Medina, 2001). For example, E. coli isolates from avian cellulitis had no affinity for fibronectin; however, given their localization on the skin suggested that they can achieve attachment via collagen (Leclerc et al., 2003) a mechanism potentially used for attachment to meat. They will also bind to type IV collagen (Selvarangan et al., 2004) primarily found in the skin within the basement of the membrane zone (Abreu-Velez and Howard, 2012).

Meat, as an important end product of livestock production, provides the muscle fibronectin (Chan et al., 2007). The mechanisms of how E. coli anchors and attaches to meat postslaughter is presented in Figure 1. Identification of the specific protein structures in the skeletal muscles, involved in adhesion, will not only help us to improve meat quality (Picard et al., 2010) but will also help us to identify the host proteins involved in pathogen binding postslaughter. E. coli strains isolated from poultry were indeed found to have a high affinity to bind fibronectin and collagen, indicating that the same isolates could be using fibronectin to bind and attach to chicken carcasses postslaughter (Gonzalez et al., 1990). Earlier data confirmed that binding to fibronectin represents indeed a mechanism of E. coli tissue adherence (Fröman et al., 1984). In vitro, binding is mediated by flagellin and GroEL (protein folding chaperone), which can be an accessory protein in this process (Moraes et al., 2015).

FIG. 1.

Escherichia coli attachment to meat. Phase 1, initial attachment (A) and the impact of oxygen (O₂), osmotic pressure (P) and temperature (T °C). Phase 2, mechanisms of attachment (B): (1) carcass, (2) E. coli cells, (3) curli, (4) type I pili, (5) type IV pili, (6) fibronectin, (7) FimH, (8) laminin, (9) carcass meat.

The STEC strain O113:H21 carries a novel type IV pilus (pil) not associated to epithelial cell attachment in vitro (Srimanote et al., 2002). Nonetheless, their role as the causing agent in the hemolytic uremic syndrome and hemorrhagic colitis was linked to their presence in retail beef in Brazil (Santos et al., 2018). The O113:H21 strain was also detected in ground beef and beef products and was genetically related to O113:H21 isolated from infectious disease cases in Australia (Feng et al., 2017). E. coli O113:H21 is also 1 of the 20 most common STEC serotypes in beef and was connected to a case of microangiopathic hemolytic anemia and thrombocytopenia in a 79-year-old female patient (Goldwater et al., 1998). Their virulence potential was revealed after the characterization of the STEC O113:H21 strain isolated from bovine cattle and retail meat in Argentina and has been identified to host the saa and stx toxinogenic genes, enabling them to cause disease in humans (Sanso et al., 2018). In a study comparing O113:H2 Irish isolates with Australian, New Zealand, and Norwegian strains it was revealed that all non-Irish isolates belonged to the O113:H21 serotype, whether the Irish isolates classified as O113:H4 serotype were lacking the saa virulence gene mentioned above in the Argentinian isolates (Monaghan et al., 2012). It was also the most prevalent serotype in bovine fecal and soil samples from 20 farms in Ireland (Monaghan et al., 2011).

The serotype O113:H4 is also strongly connected to severe disease in humans (Rahal et al., 2015) and its prevalence was estimated at 2.3% in isolates from chicken and duck hatcheries (Yousef et al., 2023). Their virulence potential, especially of those of food origin, is under constant investigation to ensure consumer protection and to further understand the link to disease. The locus enterocyte effacement (LEE) negative STEC O113:H21 strain TS18/08 isolated from minced meat, although expected to be less virulent, encoded multiple toxins expressed simultaneously (Krause et al., 2018). The LEE, a 35.6 kb pathogenicity island, expresses genes able to attach and efface lesions by intimate adherence of bacteria to enterocytes, resulting in microvilli destruction, and loss of ions followed by an onset of severe diarrhea (Franzin and Sircili, 2015). All these examples suggest that the new type IV pili expressed by E. coli O113:H21 isolated from retail meats create a less adherent phenotype that is more capable to produce toxins and cause severe disease.

Conclusion

Understanding how E. coli and specifically pathogenic E. coli will attach to meat during processing is vital to establish and implement preventive interventions. This review identified and discussed the knowledge on mechanisms of surface organelles (curli, type I and IV fimbria) involved in E. coli attachment to meat. We specifically discussed the attachment to fibrinogen, laminin, and collagen and identified that in particular E. coli meat isolates will genetically control the expression of surface organelles to ensure attachment.

Footnotes

Disclosure Statement

No competing financial interests exist.

Authors' Contributions

All authors contributed equally to the preparation of this article.

Funding Information

The publication of this article was supported by the University of Life Sciences King Mihai I from Timisoara doctoral grants.

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