Several areas around the globe experience exceptionally high incidence of Shiga toxin-producing Escherichia coli (STEC), including the virulent serotype E. coli O157:H7. These include Scotland, (Innocent et al., 2005) Ireland, (Óhaiseadha et al., 2017) Argentina, (Rivero et al., 2010) and the Canadian province of Alberta (Lisboa et al., 2019). All are home to large populations of agricultural ruminants, STEC’s primary reservoir. However, there are many regions with similar ruminant populations where STEC incidence is unremarkable. What differentiates high-risk regions is unclear. Moreover, with systematic STEC surveillance only conducted in limited parts of the world, (Kirk et al., 2015) there may be unidentified regions with exceptionally high disease burden.

STEC infections can arise from local reservoirs, transmitted through food, water, direct animal contact, or contact with contaminated environmental matrices. The most common reservoirs include domesticated ruminants such as cattle, sheep, and goats. Animal contact and consumption of contaminated meat and dairy products are significant risk factors for STEC, as are consumption of leafy greens, tomatoes, and herbs and recreational swimming that have been contaminated by feces from domestic ruminants (FAO/WHO, 2018) While STEC has been isolated from a variety of other animal species and outbreaks have been linked to species such as deer (Laidler et al., 2013) and swine, (Honish et al., 2014) it is unclear what roles they play as maintenance or intermediate hosts. STEC infections can be imported through food items traded nationally and internationally, as has been seen with E. coli O157:H7 outbreaks in romaine lettuce from the United States (Bottichio et al., 2020). Secondary transmission is believed to cause approximately 15% of cases, but transmission of the pathogen is not believed to be sustained through person-to-person transmission over the long term (Tack et al., 2021; Kintz et al., 2017).

The mix of STEC infection sources in a region directly influences public health measures needed to control disease burden. Living near cattle and other domesticated ruminants has been linked to STEC incidence, particularly for E. coli O157:H7 (Óhaiseadha et al., 2017; Jaros et al., 2013; Elson et al., 2018; Frank et al., 2008; Friesema et al., 2011; Mulder et al., 2020) These studies suggest an important role for local reservoirs in STEC epidemiology. A comprehensive understanding of STEC’s disease ecology would enable more effective investigations into potential local transmission systems and ultimately their control. Here, we take a phylodynamic, genomic epidemiology approach to more precisely discern the role of the cattle reservoir in the dynamics of E. coli O157:H7 human infections. We focus on the high incidence region of Alberta, Canada to provide insight into characteristics that make the pathogen particularly prominent in such regions.

Focusing on a region that experiences an especially high incidence of STEC, we conducted a deep genomic epidemiologic analysis of E. coli O157:H7’s multi-host disease dynamics. Our study identified multiple locally evolving lineages transmitted between cattle and humans. These were persistently associated with E. coli O157:H7 illnesses over periods of up to 13 y, the length of our study. Of clinical importance, there was a dramatic shift in the stx profile of the strains arising from locally persistent lineages toward strains carrying only stx2a, which has been associated with increased progression to hemolytic uremic syndrome (HUS) (Tarr et al., 2019).

Our study has provided quantitative estimates of cattle-to-human migration in a high-incidence region, the first such estimates of which we are aware. Our estimates are consistent with prior work that established an increased risk of STEC associated with living near cattle (Óhaiseadha et al., 2017; Jaros et al., 2013; Elson et al., 2018; Frank et al., 2008; Friesema et al., 2011; Mulder et al., 2020). We showed that 88.5% of strains infecting humans arose from cattle lineages. These transitions can be seen as a combination of the infection of humans from local cattle or cattle-related reservoirs in clade G(vi) and the historic evolution of E. coli O157:H7 from cattle in the rare clades. While our findings indicate the majority of human cases arose from cattle lineages, transmission may involve intermediate hosts or environmental sources several steps removed from the cattle reservoir. Small ruminants (e.g. sheep, goats) have been identified as important STEC reservoirs, (Elson et al., 2018; Mulder et al., 2020; Strachan et al., 2015) and Alberta has experienced outbreaks linked to swine (Honish et al., 2014). Exchange of strains between cattle and other animals may occur if co-located, if surface water sources near farms are contaminated, and through wildlife, including deer, birds, and flies (Ladd-Wilson et al., 2022; Rapp et al., 2021) Humans can also become infected from environmental sources, such as through swimming in contaminated water. Although transmission systems may be multi-faceted, our analysis demonstrates that local cattle remain an integral part of the transmission system for the vast majority of cases, even when they may not be the immediate source of infection. Indeed, despite our small sample of E. coli O157:H7 isolates from cattle, 15.7% of our human cases were within five SNPs of a cattle isolate, suggesting that cattle were a recent source of transmission, either through direct contact with the animal or their environments or consumption of contaminated food products.

The cattle-human transitions we estimated were based on structured coalescent theory, which we used throughout our analyses. This approach is similar to other phylogeographic methods that have previously been applied to E. coli O157:H7 (Franz et al., 2019). We inferred the full backbone of the Alberta E. coli O157:H7 phylogeny as arising from cattle, consistent with the postulated global spread of the pathogen via ruminants (Franz et al., 2019). Our estimate of the origin of the serotype, at 1802 (95% HPD 1731, 1861), was somewhat earlier than previous estimates, but consistent with global (1890; 95% HPD 1845, 1925) Franz et al., 2019 and the United Kingdom (1840; 95% HPD 1817, 1855) (Dallman et al., 2015) studies that used comparable methods. Our dating of the G(vi) clade in Alberta to 1969 (95% HPD 1959, 1979) also corresponds to proposed migrations of clade G into Canada from the U.S. in 1965–1977 (Franz et al., 2019). Our study thus adds to the growing body of work on the larger history of E. coli O157:H7, providing an in-depth examination of the G(vi) clade.

Our identification of the 11 locally persistent lineages (LPLs) is significant in demonstrating that the majority of Alberta’s reported E. coli O157:H7 illnesses are of local origin. Our definition ensured that every LPL had an Alberta cattle strain and at least five isolates separated by at least 1 y, making the importation of the isolates in a lineage highly unlikely. For an LPL to be fully imported, cattle and human isolates would need to be repeatedly imported from a non-Alberta reservoir where the lineage persisted over several years. Further supporting the evolution of the LPLs within Alberta, all 11 LPLs were in clade G(vi), several were phylogenetically related with MRCAs dating to the late 1990 s, and few non-Alberta isolates fell within LPLs. The nineU.S. isolates associated with Alberta LPLs may reflect Alberta cattle that were slaughtered in the U.S. or infections in travelers from the U.S. Thus, we are confident that the identified LPLs represent locally evolving lineages and potential persistent sources of disease. We also showed that the identification of these LPLs was robust to the sampling strategy, with only the smallest LPL failing to be identified after subsampling left it with <5 isolates.

We estimated the proportion of E. coli O157:H7 that were imported into Alberta in two ways. Based on our LPL analysis, we estimated only 27% of human and 10% of cattle E. coli O157:H7 isolates were imported. This was slightly higher than the overall importation estimate of 11% for all Alberta lineages from our global structured coalescent analysis. Our global structured coalescent analysis also estimated that 3% of lineages in the U.S. and 2% of lineages outside the U.S. and Canada had been exported from Alberta, suggesting that Alberta is not a significant contributor to the global E. coli O157:H7 burden beyond its borders. These results place the E. coli O157:H7 population in Alberta within a larger context, indicating that the majority of diseases can be considered local. At least one study has attempted to differentiate local vs. non-local lineages based on travel status, (Dallman et al., 2022) of which may be appropriate in some locations but can miss cases imported through food products, such as produce imported from other countries. To our knowledge, our study provides the first comprehensive determination of local vs. imported status for E. coli O157:H7 cases using external reference cases. Similar studies in regions of both high and moderate incidence would provide further insight into the role of localization on E. coli O157:H7 incidence.

Of the 11 lineages we identified as LPLs during the 2007–2015 period, six were also associated with cases that occurred during the 2016–2019 period. During the initial period, 38% of human cases were linked to an LPL, and 6% carried only stx2a. The risk of HUS increases in strains of STEC carrying only stx2a, relative to stx1a/stx2a, (Tarr et al., 2019) meaning the earlier LPL population had fewer high-virulence strains. In 2018 and 2019, the six long-term LPLs were associated with both greater incidence and greater virulence, encompassing 75% of human cases with more than half of LPL isolates carrying only stx2a. The cause of this shift remains unclear, though shifts toward greater virulence in E. coli O157:H7 populations have been seen elsewhere (Byrne et al., 2018). The growth and diversity of G(vi)-AB LPLs 2, 4, and 7 in the later period suggest these lineages were in stable reservoirs or adapted easily to new niches. Identifying these reservoirs could yield substantial insights into the disease ecology that supports LPL maintenance and opportunities for disease prevention, given the significant portion of illnesses caused by persistent strains.

The high proportion of cases associated with cattle-linked local lineages is consistent with what is known about the role of cattle in STEC transmission. Among sporadic STEC infections, 26% have been attributed to animal contact and the farm environment, with a further 19% to pink or raw meat (Kintz et al., 2017). Similarly, 24% of E. coli O157 outbreaks in the U.S. have been attributed to beef, animal contact, water, or other environmental sources (Tack et al., 2021). In Alberta, these are all inherently local exposures, given that 90% of beef consumed in Alberta is produced and/or processed there. Even person-to-person transmission, responsible for 15% of sporadic cases and 16% of outbreaks, (Tack et al., 2021; Kintz et al., 2017) includes secondary transmission from cases infected from local sources, which may explain our estimate of 11.5% of human lineages arising from other human lineages.

We developed a novel measure of persistence for use in this study, specifically for the purposes of identifying lineages that pose an ongoing threat to public health in a specific region. Persistence has been variably defined in the literature, for example, as shedding of the same strain for at least 4 mo (Barth et al., 2016). Most recently, the U.S. CDC identified the first Recurring, Emergent, and Persistent (REP) STEC strain, REPEXH01, an E. coli O157:H7 strain detected since 2017 in over 600 cases. REPEXH01 strains are within 21 allele differences of one another (https://www.cdc.gov/ncezid/dfwed/outbreak-response/rep-strains/repexh01.html), and REP strains from similar enteric pathogens are defined based on allele differences of 13–104. Given that we used high-resolution SNP analysis rather than cgMLST, we used a difference of ≤30 SNPs to define persistent lineages. While both our study and the REPEXH01 strain identified by the CDC indicate that persistent strains of E. coli O157:H7 exist, the O157:H7 serotype was defined as sporadic in a German study using the 4 mo shedding definition (Barth et al., 2016). This may be due to strain differences between the two locations, but it might also indicate that persistence occurs at the host community level, rather than the individual host level. Understanding microbial drivers of persistence is an active field of research, with early findings suggesting a correlation of STEC persistence to the accessory genome and traits such as biofilm formation and nutrient metabolism (Barth et al., 2016; Barth et al., 2020). Our approach to studying persistence was specifically designed for longitudinal sampling in high-incidence regions and may be useful for others attempting to identify sources that disproportionately contribute to disease burden. Although we used data from the reservoir species to help define the LPLs in this study, we are testing alternate approaches that rely on only routinely collected public health data.

We limited our analysis to E. coli O157:H7 despite the growing importance of non-O157 STEC, as historical multi-species collections of non-O157 isolates are lacking. As serogroups differ meaningfully in exposures, (Tarr et al., 2023) our results may not be generalizable beyond the O157 serogroup. However, cattle are still believed to be a primary reservoir for non-O157 STEC, and cattle density is associated with the risk of several non-O157 serogroups (Frank et al., 2008). Person-to-person transmission remains a minor contributor to the STEC burden. For all of these reasons, if we were to conduct this analysis in non-O157 STEC, we expect the majority of human lineages would arise from cattle lineages. Additionally, persistence within the cattle reservoir has been observed for a range of serogroups, (Barth et al., 2016) suggesting that LPLs also likely exist among non-O157 STEC. Our findings may have implications beyond STEC, as well. Other zoonotic enteric pathogens such as Salmonella and Campylobacter can persist, and outbreaks are regularly linked to localized animal populations and produce-growing operations contaminated by animal feces. The U.S. CDC has also defined REP strains for these pathogens. LPLs could shed light on how and where persistent strains are proliferating, and thus where they can be controlled.

The identification of LPLs serves multiple purposes, because they suggest the existence of local reservoir communities that maintain specific strains for long periods. First, they further our understanding of the complex systems that allow STEC to persist. In this study, the LPLs we identified persisted for 5–13 y. The reservoir communities that enable persistence could involve other domestic and wild animals previously found to carry STEC (Elson et al., 2018; Mulder et al., 2020; Strachan et al., 2015; Ladd-Wilson et al., 2022; Rapp et al., 2021; Szczerba-Turek et al., 2023). The feedlot environment also likely plays an important role in persistence, as water troughs and pen floors have been identified as important sources of STEC for cattle (Ayscue et al., 2009). Identifying LPLs is a first step in identifying these reservoir communities and determining what factors enable strains to persist, so as to identify them for targeted interventions. Second, the identification of these LPLs in cattle could identify the specific local reservoirs of STEC. Similar to source tracing in response to outbreaks, LPLs provide an opportunity for cattle growers to identify cattle carrying the specific strains that are associated with a large share of human disease in Alberta. While routinely vaccinating against STEC has not been shown to be efficacious or cost-effective, (Smith, 2014) a ring-type vaccination strategy in response to an identified LPL isolate could overcome the limitations of previous vaccination strategies. Third, the identification of new clinical cases infected with LPL strains could help direct public health investigations toward local sources of transmission. Finally, the disease burden associated with LPLs could be compared across locations and may help explain how high-incidence regions differ from regions with lower incidence.

Our analysis was limited to only cattle and humans. Had isolates from a wider range of potential reservoirs been available, we would have been able to elucidate more clearly the roles that various hosts and common sources of infection play in local transmission. Additional hosts may help explain the 1 human-to-cattle predicted transmission, which could be erroneous. As with all studies utilizing public health data, sampling from only severe cases of disease is biased toward clinical isolates. In theory, this could limit the genetic variation among human isolates if virulence is associated with specific lineages. However, clinical isolates were more variable than cattle isolates, dominating the most divergent clade A, so the overrepresentation of severe cases does not appear to have appreciably biased the current study. Similarly, in initially selecting an equal number of human and cattle isolates, we sampled a larger proportion of the human-infecting E. coli O157:H7 population compared to the population that colonizes cattle. As cattle are the primary reservoir of E. coli O157:H7, the pathogen is more prevalent in cattle than in humans, who appear to play a limited role in sustained transmission. In sampling a larger proportion of the strains that infect humans, we likely sampled a wider diversity of these strains compared to those in cattle, which could have biased the analysis toward finding humans as the ancestral host. Thus, the proportion of human lineages arising from cattle lineages (88.5%) might be underestimated, which is also suggested by our sensitivity analysis of equal numbers of cattle and clinical isolates. Finally, we were not able to estimate the impact of strain migration between Alberta and the rest of Canada, because locational metadata for publicly available E. coli O157:H7 sequences from Canada was limited.

E. coli O157:H7 infections are a pressing public health problem in many high-incidence regions around the world including Alberta, where a recent childcare outbreak caused >300 illnesses. In the majority of sporadic cases, and even many outbreaks, (Tack et al., 2021) the source of infection is unknown, making it critical to understand the disease ecology of E. coli O157:H7 at a system level. Here, we have identified a high proportion of human cases arising from cattle lineages and a low proportion of imported cases. Local transmission systems, including intermediate hosts and environmental reservoirs, need to be elucidated to develop management strategies that reduce the risk of STEC infection. In Alberta, local transmission is dominated by a single clade, and over the extended study period, persistent lineages caused an increasing proportion of disease. The local lineages with long-term persistence are of particular concern because of their increasing virulence, yet they also present opportunities as larger, more stable targets for reservoir identification and control.

Sequencing data have been deposited in SRA. Accession numbers and deidentified metadata for all sequences used, including existing sequences and those sequenced for this study, are listed in the Source Data.

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Author details

1. Gillian AM Tarr

   Division of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, United States

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Funding acquisition, Visualization, Methodology, Writing – original draft

   For correspondence

   gtarr@umn.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7372-1034

2. Linda Chui

   1. Alberta Precision Laboratories, Alberta Public Health, Walter Mackenzie Health Sciences Centre, Edmonton, Canada
   2. Department of Laboratory Medicine and Pathology, University of Alberta, Edmonton, Canada

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

3. Kim Stanford

   Department of Biological Sciences, University of Lethbridge, Lethbridge, Canada

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

4. Emmanuel W Bumunang

   Department of Biological Sciences, University of Lethbridge, Lethbridge, Canada

   Contribution

   Data curation, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

5. Rahat Zaheer

   Agriculture and Agri-Food Canada, Lethbridge Research and Development Centre, Lethbridge, Canada

   Contribution

   Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

6. Vincent Li

   Alberta Precision Laboratories, Alberta Public Health, Walter Mackenzie Health Sciences Centre, Edmonton, Canada

   Contribution

   Data curation, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

7. Stephen B Freedman

   Sections of Pediatric Emergency Medicine and Gastroenterology, Department of Pediatrics, Alberta Children’s Hospital and Alberta Children’s Hospital Research Institute, Cumming School of Medicine, University of Calgary, Calgary, Canada

   Contribution

   Conceptualization, Funding acquisition, Project administration, Writing – review and editing

   Competing interests

   No competing interests declared

8. Chad R Laing

   National Center for Animal Diseases Lethbridge Laboratory, Canadian Food Inspection Agency, Lethbridge County, Canada

   Contribution

   Conceptualization, Funding acquisition, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

9. Tim A McAllister

   Agriculture and Agri-Food Canada, Lethbridge Research and Development Centre, Lethbridge, Canada

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Methodology, Project administration, Writing – review and editing

   Competing interests

   No competing interests declared

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