Case Ascertainment, 1983–2012

Beginning in 1983, only fecal specimens from patients with HUS or hemorrhagic colitis were referred for STEC O157 testing; before 1989, few specimens were referred for testing. Beginning in 1997 in England and Wales, referral for testing was extended to all patients with symptoms of gastrointestinal infection, including vomiting, diarrhea, or bloody feces.

Microbiology Methods, 1983–2012

GBRU provides the national reference service for STEC in England and Wales. Beginning in 1983, individual colonies were tested for toxin production by using the verocytotoxin cell assay, and positive colonies were identified biochemically and serotyped (13). In 1987 at GBRU, the verocytotoxin cell assay was replaced with a molecular probe assay to detect the stx gene (14) and sorbitol MacConkey culture medium. Later, sorbitol MacConkey culture medium containing cefixime and tellurite was developed, facilitating isolation of STEC O157 from fecal specimens, but testing was not implemented for all patients with symptoms of gastrointestinal infection in all local hospital laboratories until 1997 (15). Isolates of E. coli O157 identified locally are sent for confirmation and typing at GBRU.

Detection and confirmation of STEC at GBRU includes biochemical identification and serotyping of bacterial isolates. Since 1989, strains belonging to E. coli O157 have been further differentiated by using a phage typing scheme developed in Canada (16). Retrospective phage typing was undertaken for all viable strains collected before 1989. During 1994–2011, detection of stx1 or stx2 used a block-based PCR (17), which was replaced in 2012 with real-time PCR targeting stx1 or stx2 and the intimin (eae) gene, associated with intimate attachment of the bacteria to the host gut mucosa (18).

Data Collection Methods, 1983–2012

The amount of epidemiologic and microbiological data increased during the study period. During 1983–2003, a dedicated laboratory database was used to record patient and microbiological data. In 2004, a new laboratory reporting system, Modular Open Laboratory Information System, was implemented (Figure 1). These laboratory databases captured microbiological results and demographic details of cases, as well as limited epidemiologic data (HUS diagnosis, outbreak association, recent history of foreign travel).

In January 2009, PHE introduced the National Enhanced Surveillance Scheme for STEC (Figure 1) (19). This scheme captured epidemiologic information through standardized questionnaires administered to all persons with STEC and linked to microbiological data in the Modular Open Laboratory Information System.

Detection of outbreaks relied on detecting unusual increases in STEC activity or reporting of shared exposures among cases of the same phage type (PT). Outbreaks were recorded on paper before 1992. In 1992, PHE began standardized surveillance of outbreaks of gastrointestinal disease where >2 persons with the same infection are linked, or probably linked, to the same source. In brief, local PHE units report standardized epidemiologic data on all outbreaks of gastrointestinal diseases, including source of infection and microbiological data.

Data Analyses

Data on STEC O157 patients in England and Wales were analyzed in 3 time periods, 1983–1988, 1989–1996, and 1997–2012, to account for periods of differing case ascertainment and data collection. Case numbers for 1989–1996 were small and represent biased sampling toward severe STEC O157 infections therefore calculation of incidence and interpretation of trends would be meaningless, and these were calculated only for 1997–2012.

We performed descriptive analyses in Microsoft Excel 2010 (Microsoft Corporation, Redmond, WA, USA). Crude incidence rates were calculated by using the Office of National Statistics mid-year population estimates (20). Crude incidence rate ratios (RR) and 95% CIs were calculated in Stata version 13.0 (StataCorp LP, College Station, TX, USA) for comparison among groups.

Microbiology of STEC O157, 1983–2012

In England and Wales during 1983–1988, a total of 279 patients were infected with STEC O157, including 110 from 3 outbreaks. Of the 169 non–outbreak-related isolates, 155 were retrospectively phage typed; the most common types were PT2 (49 [31.6%] cases), PT1 (38 [24.5%]), and PT49 (22 [14.2%]).

Figure 2

Figure 2. Proportions of common phage types (PTs) of Shiga toxin–producing Escherichia coli O157 identified, England and Wales, 1989–2012.

During 1989–1996, the number of cases increased (3,448 total cases), and the proportions of common PTs changed annually (Figure 2). In 1996, a new PT was designated PT21/28 after reexamination of the lysis profiles of PT21 and PT28 isolates (21). By 1996, PT2 (244 [37%] isolates), PT8 (85 [12.9%] isolates), and PT21/28 (92 [13.9%] isolates) were the most common PTs, and the proportion of PT1 (28 [4.2%] isolates) and PT49 (42 [6.4%] isolates) had declined.

During 1997–2012, the decline in these PTs continued, and PT1 and PT49 were rarely observed. PT2 also declined to just 28 (3.4%) isolates by 2012 from a peak of 430 (54.3%) isolates in 1995, a significant decrease for this period (p<0.001) (Figure 2). Concurrently, numbers of PT21/28 rapidly increased, accounting for 420 (44.1%) cases by 2005, a significant increase for the period (p<0.001), and thereafter remaining the most frequently detected PT (Figure 2). PT8 also increased significantly, from 182 (16.7%) to 225 (27.5%) of cases by 2012 (p<0.001).

Strains encoding Stx1 only were rare (81 [0.6%] isolates), and most (45 [55.6%] isolates) were PT8. Strains encoding Stx2 only were most frequent (10,182 [71.8%] isolates), followed by Stx1+2 (3,921 [27.6%] isolates). Stx type and PT are interrelated; most PT8 strains (3,040 [93.2%] isolates) possessed stx1+2, whereas PT2 and PT21/28 usually possessed stx2 only (2,100 [92.8%] and 4,340 [99.7%] isolates, respectively).

Epidemiology of STEC O157, 1997–2012

Case Numbers and Crude Incidence

Figure 3

Figure 3. Crude incidence (cases per 100,000 person-years) of Shiga toxin–producing Escherichia coli O157, by patient age group and sex, England and Wales, 1997–2012. Error bars indicate 95% CIs.

A total of 14,184 laboratory-confirmed STEC O157 cases were identified in England and Wales; the mean was 887 (95% CI 802–972) cases per year. Crude incidence was 1.65 (95% CI 1.49–1.81) cases/100,000 person-years but varied by year, geography, and patient age and sex (Figure 3). Identifiable peaks in case numbers corresponded to reported outbreaks (Figure 1; Table). Crude incidence decreased from 1999, reaching its lowest in 2002 (1.1 cases/100,000 person-years [595 cases]), but returned to previous levels in 2005 and was sustained thereafter.

STEC O157 infections demonstrated a distinct seasonality. Cases began to increase in April and declined beginning in September (data not shown).

Outbreaks, 1983–2012

During 1983–2012, a total of 335 outbreaks were reported, ranging from 0 to 25 outbreaks annually (Table). These outbreaks constituted 3,107 (17.4%) cases (median 5 cases, range 2–257 cases).

Large outbreaks caused peaks in annual crude incidence (Figure 1). For example, in 1995, eleven outbreaks comprising 141 cases occurred (Table), including a large nursery outbreak in Wales affecting 49 children (6). In 1999, nineteen outbreaks (236 cases) occurred, causing incidence to peak. Nine were attributed to contaminated food vehicles, including 3 caused by milk pasteurization failures, 1 affecting 88 persons (22). Outbreaks caused by postpasteurization contamination of milk also occurred in 2000 and 2002, as did 2 outbreaks associated with drinking raw milk in 2000, but no milk-related outbreaks were observed during the remainder of the study period.

Food vehicles contributed the highest number of outbreaks (101 [30.3%]) and outbreak cases (1,418 [45.9%]) (Table). These outbreaks included 38 attributed to eating contaminated meat; 16 to eating undercooked meat, such as burgers at barbecues; and 22 to cross-contamination of cooked meats. The cross-contamination outbreaks were larger; the largest meat-related outbreak occurred in Wales when meat from a butcher supplied to institutions infected 118 persons with STEC O157 in 2005 (12). After that, meat-related outbreaks were infrequent; 7 meat-related outbreaks (compared with 31 before this outbreak) were reported in the subsequent 7 years.

The first implicated food vehicle in this study was raw potatoes in a 1985 outbreak, and outbreaks associated with eating vegetables were reported throughout the years. The largest national outbreak in Great Britain (252 cases) caused by STEC O157 PT8, linked to handling raw leeks and potatoes, was reported in 2011 and led to the highest incidence during the period (Figure 1) (23).

Person-to-person spread in institutional settings accounted for 29.1% of outbreaks and more than one quarter of outbreak cases (825 cases). Twenty-six outbreaks occurred in institutional settings: care homes (16 outbreaks), prisons (4 outbreaks), and hospitals (6 outbreaks). No outbreaks in these settings occurred after 2007. Seventy-two outbreaks, which resulted in 808 cases, occurred in childcare facilities. Each year, 1–7 outbreaks in child-care facilities occurred, but outbreaks increased in frequency in later years; during 1983–2003, a total of 25 outbreaks (313 cases) were reported, whereas 47 outbreaks (495 cases) were reported in the subsequent 9 years.

Direct or indirect contact with animals through the environment accounted for 22.4% of outbreaks and 17.3% of patients linked to outbreaks. The number of petting farm outbreaks increased during the study period. During 1983–2002, a total of 12 petting farm outbreaks were reported; during 2003–2012, a total of 31 outbreaks on petting farms were reported, including, in September 2009, the largest reported farm outbreak, which affected 93 persons (9).

Most outbreaks were caused by the most frequently detected STEC O157 PTs, including PT21/28 (117 [34.9%] outbreaks), PT2 (79 [23.6%] outbreaks), and PT8 (42 [12.5%] outbreaks). In accordance with the general trends in PT, PT2 outbreaks declined over time, whereas PT8 and PT21/28 outbreaks increased. For outbreaks attributed to contact with animals or their environments, almost half (28 [47.5%] outbreaks) were caused by PT21/28 strains, a further 16 (27.1%) by PT2 strains, and only 4 (6.8%) by PT8 strains. Ten outbreaks attributed to contaminated water were caused by PT2 (5 outbreaks), PT21/28 (4 outbreaks), and PT4 (1 outbreaks); none were caused by PT8. In foodborne outbreaks, 25 (28.1%) were caused by PT2, 32 (36.1%) by PT21/28, and 20 (22.5%) by PT8.