School outbreak of Escherichia coli O157 with high levels of transmission, Staffordshire, England, February 2012

Journal of Public Health Vol. 38, No. 3, pp. e247 e253 doi:10.1093/pubmed/fdv122 Advance Access Publication September 12, 2015 School outbreak of Escherichia coli O157 with high levels of transmission, Staffordshire, England, February 2012 Laura Bayliss 1, Robert Carr 2, Obaghe Edeghere 1, Elizabeth Knapper 2, Kathy Nye 3, Gareth Harvey 4, Goutam Adak 5, Harsh Duggal 2 1 Field Epidemiology Service, Public Health England, Birmingham, UK 2 Health Protection Team North, Public Health England Centre West Midlands, Public Health England, Birmingham, UK 3 Public Health Laboratory Birmingham, Public Health England, Birmingham, UK 4 Environmental Health Department, Newcastle-under-Lyme Borough Council, Stoke-on-Trent, UK 5 Gastrointestinal Emerging and Zoonotic Infections, Centre for Infectious Disease Surveillance and Control, Public Health England, London, UK Address correspondence to Obaghe Edeghere, E-mail: obaghe.edeghere@phe.gov.uk ABSTRACT Background Verocytotoxin-producing Escherichia coli (VTEC) are bacteria that cause infectious gastroenteritis and in certain settings can cause widespread infection due to secondary transmission. We describe the findings of an investigation of a school-based outbreak of VTEC in Staffordshire, England. Methods Outbreak investigation at a school in February 2012 after two children were diagnosed with VTEC infection. Cases were defined as pupils and staff (or their household contacts) with gastrointestinal symptoms or asymptomatic screened persons, with laboratory confirmed VTEC O157 infection ( phage type 32, verocytotoxin 2) occurring on or after 1 February 2012. Microbiological tests of food and faecal samples plus screening of asymptomatic contacts were undertaken. Epidemiological and clinical data were descriptively analysed. Results Thirty-eight cases were detected. Nineteen were asymptomatic and identified via screening of 191 pupils. Infection was introduced into the school from an earlier household cluster, followed by extensive person-to-person transmission within the nursery/infant group with limited spread to the wider school population. Conclusions Control measures included several interventions, in particular, universal screening of pupils and staff. Screening during school outbreaks is not underpinned by guidance but proved to be a key control measure. Screening of asymptomatic contacts should be considered in similar outbreaks. Keywords communicable diseases, epidemiology, public health Introduction Verocytotoxin-producing Escherichia coli (VTEC) are bacteria that cause infectious gastroenteritis. Although VTEC infection has a low incidence in the UK, it remains an important public health problem for the following reasons. Low infectious dose needed to cause disease 1 ; occurrence of complications like haemolytic-uraemic syndrome (HUS), fatalities among vulnerable groups 2 and the potential for widespread infection from secondary transmission in certain settings. 3 In England and Wales, national surveillance undertaken between 2007 and 2011 showed around 1000 VTEC cases reported annually with a crude incidence of 1.7 cases per 100 000 population. 4 Outbreaks in various settings including schools account for a fifth of all cases reported in England and Wales annually. 5 In nurseries/primary schools, person-to-person spread is common, leading to high secondary transmission Laura Bayliss, Information Scientist Robert Carr, Consultant in Communicable Disease Control Obaghe Edeghere, Consultant Epidemiologist Elizabeth Knapper, Senior Health Protection Nurse Kathy Nye, Consultant Microbiologist Gareth Harvey, Environmental Health Team Manager Goutam Adak, Head of Gastrointestinal Infection Surveillance Harsh Duggal, Consultant in Communicable Disease Control # Crown copyright 2015. e247

e248 JOURNAL OF PUBLIC HEALTH rates during outbreaks involving children with a median age of,6 years. 3 Between 2009 and 2011, 12 VTEC O157 outbreaks occurred in nursery/school settings in England, representing the third largest proportion of outbreak-related cases (15%) after general community outbreaks (34%) and outbreaks linked to visits to working farms and petting farm animals (24%). 6 In Staffordshire, England, a suspected outbreak of VTEC O157 involving two pupils at a primary school was notified to the local Health Protection Team (HPT) in March 2012. Over the coming days, further suspected cases were reported among pupils and household contacts. A multi-agency outbreak control team (OCT) convened to investigate the outbreak in order to determine the size and cause and identify effective control measures. We present findings from the outbreak investigation and describe key lessons from the response. Methods Setting The outbreak occurred at a primary school with 184 pupils and 38 staff located in Staffordshire. Staffordshire is in the North East of the West Midlands region of England and has a population of 840 000. 7 The primary school is managed by the Local authority (administrative body) and pupils are taught in two-year groups: the nursery/infant (for 3- to 6-year olds) and junior (for 7- to 11-year olds) groups. Epidemiological investigation The case definition from national guidance 8 was adopted and modified with increasing specificity as the investigation progressed. Confirmed cases were pupils, staff members or household contacts of pupils/staff with gastrointestinal symptoms and laboratory confirmed VTEC O157, phage type (PT) 32, verocytotoxin (VT) 2 or asymptomatic screened persons with laboratory confirmed VTEC O157, PT32, VT2 occurring on or after 1 February 2012. Secondary cases were defined as persons with an epidemiological link to a primary case(s) where it was more likely that the individual was infected at home or other settings. Passive case finding was undertaken by informing nearby general practices and local hospitals and press statements were issued through local newspapers and television media to raise awareness of the outbreak among the general public. Letters were sent to parents of pupils and school staff. Environmental Health Officers (EHOs) used a standardized questionnaire to collect demographic, clinical and epidemiological data with additional data on attendance at the pre and after school club obtained from the school s administrative records. Parents/guardians gave verbal consent and completed the questionnaires on behalf of their ward(s). No sample size calculation was undertaken as analysis was based on all outbreak cases. We described the outbreak in time, place and person and calculated year group specific attack rates (ARs) for exposure to school meals and the pre/after school club. Fisher s exact test was used to calculate risk ratios (RRs) and 95% confidence intervals for the association between infection and attendance at the pre/after school club as well as school meal consumption during a hypothesized exposure period. This exposure period was estimated as 21 24 February 2012 based on the earliest peak in cases and the median incubation period for VTEC O157. Multivariable analysis was not undertaken as it was deemed unnecessary although a plan had been developed a priori. All analyses were undertaken using Microsoft Excel and STATA 11 (StataCorp, USA). Microbiological investigation Symptomatic cases and asymptomatic pupils and staff that participated in the school-wide VTEC screening provided faecal specimens. Specimens were tested at the Health Protection Agency (HPA) West Midlands Public Health Laboratory, Birmingham (HPA is now part of Public Health England). VTEC O157 tests were in accordance with UK National Standard Microbiology Investigations 9 including an enrichment step in Tryptone Soy Broth to improve the diagnostic yield of samples with low numbers of viable organisms. A polymerase chain reaction (PCR) test was used to confirm presumptive isolates and identify the presence of specific VT genes (VT 1 and 2). Confirmed isolates were sent to the HPA Laboratory of Gastrointestinal Pathogens, London for phage typing and DNA analysis using variable number tandem repeat (VNTR) analysis to characterize the strains. Initial specimens from symptomatic cases were also tested for Salmonella, Shigella and Campylobacter. Environmental investigation EHOs visited the school on 2 March and inspected the toilets, main kitchen facility and a separate kitchen facility used by the pre/after school club to assess compliance with extant regulations. Environmental samples were not collected as the school kitchen, toilets and classrooms had undergone enhanced cleaning and disinfection. Food items were not sampled from the kitchen as none remained from the period preceding the outbreak and inspection showed high standards of food hygiene. On 26 March, EHOs obtained for testing, samples of raw carrot sticks distributed to the infant group as part of a national

SCHOOL OUTBREAK OF ESCHERICHIA COLI O157 e249 free fruit and vegetables scheme. Trace back of the school s food supply chain and the national fruit and vegetables scheme was undertaken to ascertain whether any cases had been reported in other schools/settings that shared supplier(s). School-based VTEC screening VTEC screening was conducted to support case finding, determine carriage rates within the school and inform decisions around return to school. Collection of faecal specimen at the school was coordinated by EHOs who attended daily from 8 11 March 2012 and pupils continued to send in specimen until 18 April when screening ended. Health protection staff attended the school on three consecutive days to respond to any questions from parents. Children 7 years old had to provide a minimum of two faecal specimen at least 24 h apart and older children/adults provided at least one specimen. This was based on the higher risk of infection, transmission and untoward outcomes in children aged 6 years old compared with older children/adults. 10 Screening results were communicated via the following routes depending on the results: (a) Initial phone call from the HPT if positive followed by a letter. (b) Letter from the HPT informing of a negative result. We calculated the laboratory costs of screening using National Health Service standard tariffs but did not estimate the resource requirements in terms of man hours. Results Two hundred and twenty-one people from thirty-two households, mainly children, were tested for VTEC O157 infection. Of these, thirty-eight (17%) were positive for VTEC O157 (PT32/VT2). Nineteen (8.5%) were symptomatic and 19 were asymptomatic persons detected during screening. Eleven symptomatic individuals tested negative for VTEC O157. Screening uptake at the school was 86% (191/221) with seven pupils unscreened because they were out of the country. The majority of symptomatic confirmed cases had an onset between 25 February and 6 March (Fig. 1). Among symptomatic cases, 10/19 (53%) reported non-bloody diarrhoea and 7/19 (37%) bloody diarrhoea. Eight and two cases reported stomach cramps and vomiting, respectively. Three cases were seen for care in hospital (two admitted and one assessed) and were discharged with no complications reported (Table 1). Confirmed cases ranged in age from 1 to 56 years (median ¼ 5 years) with 20 (53%) male cases (Table 1). Cases were mostly pupils at the school (79%; 30/38) and the microbiologically confirmed AR at the school was 15% (32/215). There were 29 cases among pupils in the nursery/infant year group, the highest AR (27.1%; 95% CI 19.6 36.2) (Table 2). There was only one confirmed case in the junior year group (AR ¼ 1.4%, 95% CI 0.3 7.7) and two asymptomatic cases were identified among the teaching/teaching support staff (AR ¼ 5.2%, 95% CI 1.5 17.3) (Table 2). Both staff were linked to the nursery/infant year and one had two children identified as carriers through screening. Six cases were reported among close household-type contacts with epidemiological links to a case at the school. One household case had the earliest onset date and was part of a household cluster that included two pupils, one of whom was the first case identified at the school. Information on the clinical status of pupils when they last attended the school was available for 46% (18/38) of cases, and showed that five symptomatic pupils attended school Number confirmed 6 5 4 3 2 1 0 Household Infant Junior 01/02/2012 03/02/2012 05/02/2012 07/02/2012 09/02/2012 11/02/2012 13/02/2012 15/02/2012 17/02/2012 19/02/2012 21/02/2012 23/02/2012 25/02/2012 Oneset date School closed 27/02/2012 29/02/2012 02/03/2012 04/03/2012 06/03/2012 08/03/2012 10/03/2012 12/03/2012 14/03/2012 Fig. 1 Epidemic curve of all symptomatic laboratory confirmed cases (excludes 11 symptomatic cases that were VTEC negative on testing) by case category, 1 February to 14 March 2012 (n ¼ 19).

e250 JOURNAL OF PUBLIC HEALTH Table 1 Selected characteristic of laboratory confirmed VTEC cases by case category, Staffordshire, 1 February to 9 March 2012 (n ¼ 38) Selected characteristic Primary case (n ¼ 31) Secondary case (n ¼ 7) All cases (n ¼ 38) Sex Male 15 (48%) 5 (71%) 20 (53%) Female 16 (52%) 2 (29%) 18 (47%) Median age (range) 5 years (3 56) 6 years (1 27) 5 years (1 56) Hospitalized 2 (6%) 1 (14%) 3 (8%) Case group Nursery/infant 26 (84%) 3 (43%) 29 (76%) Junior 0 1 (14%) 1 (3%) Staff 2 (6%) 0 2 (5%) Household 3 (10%) 3 (43%) 6 (16%) Attended pre and 13 (50%) 3 (75%) 16 (42%) after school club a Reported eating a school meal b 25 (96%) 3 (75%) 28 (73%) a Defined as attending the pre and after school club on at least one occasion during the hypothesized period of exposure (21 24 February 2012). b Defined as consuming a school meal on at least one occasion during the hypothesized period of exposure (21 24 February 2012). Table 2 Number of laboratory confirmed VTEC cases (symptomatic and asymptomatic) and ARs (%) by school group (n ¼ 32) Number of cases Population at risk AR % 95% CI Infants/nursery 29 107 27.1 19.6 36.2 Junior 1 70 1.4 0.3 7.7 Staff 2 38 5.3 1.5 17.3 School 32 215 14.8 AR, attack rate. whilst unwell. Where information was available for asymptomatic cases (6/19; 31.5%), all reported attending school until the day it was voluntarily closed. Overall, 113 of 177 pupils reported consuming a school meal and 72 of 177 pupils reported attending the pre/after school club during the hypothesized exposure period. Reporting consuming a school meal was significantly associated with increased risk of infection (RR ¼ 7.9, 95% CI 1.9 32.1; P ¼ 0.0001). However, this association was only statistically significant in the nursery/infant and not the junior group when stratified by year group (Table 3). There was a positive but non-significant association between reported attendance at the pre and after school club and infection (RR ¼ 1.67; 95% CI 0.9 3.2; P ¼ 0.12) (Table 4). Twenty-one clinical isolates were sent for VNTR profiling. Twenty had an indistinguishable profile and one (a household case) was a single locus variant. Microbiological tests undertaken on samples of raw carrot sticks provided to the nursery/infant group as part of a free fruit and vegetables scheme were negative for VTEC O157. Control measures A range of control measures were implemented in response to the outbreak: (1) Dissemination of written and verbal information to parents, guardians, general public and the local media to raise awareness and provide advice (2) Enhanced cleaning regime at the school and a deep clean (3) Supervised hand washing for pupils in the nursery/infant year group (4) Screening of all asymptomatic pupils and staff with the following actions taken based on the results of the tests: Asymptomatic, screen negative can return to school Aged 7 years old with evidence of infection, school exclusion to continue until microbiological clearance (defined as two negative VTEC faecal samples taken at least 48 h apart) Staff members in a risk group (e.g. caterers/food handler) with evidence of infection, school exclusion to continue until microbiological clearance Older children unable to maintain adequate levels of enteric hygiene with evidence of infection, exclusion to continue until microbiological clearance (5) Cancellation of all school trips (6) Voluntary school closure on 7 March 2012 The school reopened on 21 March 2012 with a phased reintroduction of screen negative pupils into the school. Most control measures remained operational until the outbreak was declared over when the last screen positive pupil was cleared to return to school on 26 April 2012. Costs During the outbreak, 597 faecal samples related to this outbreak were processed, 374 were received in the first week. Based on a processing cost of 16 per sample, laboratory tests alone cost 9552. Discussion Main findings of the study This was the largest school outbreak of VTEC O157 identified in West Midlands, England.

SCHOOL OUTBREAK OF ESCHERICHIA COLI O157 e251 Table 3 Relative risk of E. coli infection (and 95% confidence intervals) for pupils reporting consuming a school meal between 21 and 24 February 2013, Staffordshire (n ¼ 177) Consumption of school meal a RR 95% CI P-Value Exposed Unexposed Cases b Non-cases AR % Cases b Non-cases AR % All pupils 28 85 24.8 2 62 3.1 7.9 1.9 32.1 0.002 Nursery/infant 27 40 40.3 2 38 5.0 8.0 2.0 32.0 0.0001 Junior 1 45 2.2 0 24 0 n.c. n.c. 0.466 AR, attack rate; RR, risk ratio; CI, confidence interval; n.c., not computable. All estimates derived using Fisher s exact test. a Defined as consuming a school meal on at least one occasion during the hypothesized period of exposure (21 24 February 2013). b Laboratory confirmed cases only (symptomatic and asymptomatic screen positives). Table 4 Relative risk of E. coli infection (and 95% confidence intervals) for pupils that attended the pre and after school club between 21 and 24 February 2013, Staffordshire (n ¼ 177) Attendance at pre and after school club a RR 95% CI P-Value Exposed Unexposed Cases b Non-cases AR % Cases b Non-cases AR % All pupils 16 56 22.2 14 91 13.3 1.67 0.9 3.2 0.12 Nursery/infant 15 34 30.6 14 44 24.1 1.2 0.7 2.4 0.45 Junior 1 22 4.3 0 47 0 n.c. n.c. 0.15 AR, attack rate; RR, risk ratio; CI, confidence interval; n.c., not computable. All estimates derived using Fisher s exact test. a Defined as attending the pre and after school club on at least one occasion during the hypothesized period of exposure (21 24 February 2013). b Laboratory confirmed cases only (symptomatic and asymptomatic screen positives). Pupils aged,6 years of age experienced the greatest burden of illness with extensive person-to-person transmission in this age group and limited spread to the wider school population. Symptomatic infections were mild and selflimiting with no reports of complications such as HUS. Screening of asymptomatic pupils and staff identified carriers in 1 in 10 pupils aged,6 years of age. Epidemiological and microbiological findings supported a hypothesis that the pathogen was introduced into the school from a case that was part of an earlier household cluster, with subsequent transmission within the school. The outbreak strain (VTEC O157, PT32/VT2) identified among cases was indistinguishable by VNTR profiling. The genetic relatedness of clinical isolates and identification of the outbreak strain in the purported index case, a symptomatic adult household contact of a pupil, both of whom reported symptoms that predated the onset of illness in other pupils provided further support for the hypothesis. Our findings indicate a low likelihood of point source exposure to contaminated food and/or water. Although there was a statistically significant association between infection and reporting consuming school meals; this was only observed in the nursery/infant year. We do not think this indicates exposure to contaminated food as all pupils were served the same meals in the same settings and pupils in the junior year were no less likely to have reported consuming a school meal during the hypothesized exposure period. In addition, schools in the same Local Education Authority (LEA) area that used the same company that supplied food to the school, or the free fruit and vegetable programme did not report any VTEC cases during this period. Furthermore, laboratory tests on samples of carrots provided to the school as part of the programme were negative for VTEC O157. What is already known on this topic? The age distribution of carriers identified through screening in this outbreak is consistent with existing literature which report higher levels of asymptomatic carriage amongst young children, 11,12 a group also more likely to shed the bacteria in

e252 JOURNAL OF PUBLIC HEALTH their faeces for a prolonged period of time. 10,13 These and other factors such as mixing patterns at the school and suboptimal levels of enteric hygiene are known to contribute to the increased risk of secondary spread in this type of setting 10 thus increasing the potential for outbreaks and undetected transmission in this vulnerable population. In England, this outbreak strain is uncommon and accounts for 6% of laboratory confirmed cases annually over a 5-year period 4 and has not been identified in any previous outbreaks. In Ireland, a school outbreak caused by a similar strain shared certain characteristics with this outbreak with high levels of person-to-person transmission and asymptomatic carriage. 12,14 What this study adds The multi-agency OCT agreed measures to control the outbreak, in particularly, the screening of all asymptomatic pupils and staff for carriage with positive individuals returning to school only after microbiological clearance. Guidance by the HPA (now part of Public Health England) that was extant at the time of the outbreak recommends exclusion and microbiological clearance of cases in at-risk groups but not universal screening of the school population. 8 The use of universal screening resulted in the identification of half the VTEC positive pupils associated with this outbreak, carriers that would have been missed with the attendant risk of continuing transmission. The absence of carriers amongst screened pupils in the junior group raised questions about the best approach to screening in these circumstances. Screening the entire school was a disruptive process and the direct and intangible costs to parents looking after sick/excluded children can be considerable. 15,16 As there is good evidence that younger children are more likely to be asymptomatic shedders 10,11,15,17 ; a targeted approach may have achieved the same impact whilst minimizing any disruption experienced by parents and pupils during the screening exercise. The closure of the school was an independent decision taken by the school but this facilitated the deep clean of the premises and the gradual return of pupils to school in a manner that reduced the risk of on-going transmission in the school as no further cases were reported when the school reopened. However, there were additional challenges for pupils, parents and the OCT as the need for microbiological clearance of excluded pupils created additional child care burden for the affected households and a huge logistic exercise for the health protection and environmental health teams who co-ordinated the screening. Limitations of this study We could not investigate the potential role of environmental contamination in this outbreak as no environmental samples were collected. Studies report that VTEC O157 can survive on a range of materials and under various conditions for long periods of time, 18 and the risk of infection from environmental contaminants is widely reported, especially considering the low infectious dose required to cause illness. 1 Therefore, it is plausible that contamination of the school environment could have played a role in disease transmission. We sampled carrots several weeks after the start of the outbreak and acknowledge that these are unlikely to be from the same batch that the school received prior to the outbreak. However, free fruit was also supplied to other schools in the LEA area and no other cases were reported. Conclusions This large school-based outbreak of VTEC O157 was characterized by extensive person-to-person transmission and asymptomatic carriage in children aged,6 years which was underpinned by findings from molecular testing of clinical isolates. The utility of screening asymptomatic school contacts was considerable as we detected several asymptomatic carriers at the school. However, the universal screening approach we adopted was disruptive and challenging. Although the evidence base that supports the use of screening in managing school outbreaks is limited, such an approach should be considered in future outbreaks in similar settings. Supplementary data Supplementary data are available at PUBMED online. Authors contributions L.B. contributed to the outbreak investigation and drafted the manuscript as the lead author; R.C. led the outbreak investigation and drafted the manuscript as a co-author; O.E., E.K., G.H., K.N., G.A. and H.D. contributed to the outbreak investigation and drafted the manuscript as co-authors. Acknowledgements We are grateful to all the members of the OCT: Public Health England (PHE) West Midlands North Health Protection Team, West Midlands Field Epidemiology Team, West Midlands Public Health Laboratory, University Hospital North Staffordshire Microbiology Department, EHOs at Newcastle-under-Lyme Borough Council, Staffordshire County Council s Education department, Gastrointestinal & Zoonotic Infections Unit (GEZI) and staff members and parents of pupils at the Primary School.

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