key: cord-1035842-nl2rt551 authors: Love, N. K.; Elliot, A. J.; Chalmers, R.; Douglas, A.; Gharbia, S.; McCormick, J.; Hughes, H.; Morbey, R.; Vivancos, R.; Smith, G. title: The impact of the COVID-19 pandemic on gastrointestinal infection trends in England, February - July 2020 date: 2021-04-07 journal: nan DOI: 10.1101/2021.04.06.21254174 sha: 4486b2214d64caa366af462cdcb4fa1ff4d8213d doc_id: 1035842 cord_uid: nl2rt551 Objective: To establish the impact of the first six months of the COVID-19 outbreak response of gastrointestinal (GI) infection trends in England. Design: Retrospective ecological study using routinely collected national and regional surveillance data from eight Public Health England coordinated laboratory, outbreak and syndromic surveillance systems using key dates of UK governmental policy change to assign phases for comparison between 2020 and historic data. Results: Decreases in GI illness activity were observed across all surveillance indicators as COVID-19 cases began to peak. Compared to the 5-year average (2015-2019), during the first six months of the COVD-19 response, there was a 52% decrease in GI outbreaks reported (1,544 vs. 3,208 (95% CI: 2,938 - 3,478) and a 34% decrease in laboratory confirmed cases (27,859 vs. 42,495 (95% CI: 40,068 - 44,922). GI indicators began to rise during the first lockdown and lockdown easing, although all remained substantially lower than historic figures. Reductions in laboratory confirmed cases were observed across all age groups and both sexes, with geographical heterogeneity observed in diagnosis trends. Health seeking behaviour changed substantially, with attendances decreasing prior to lockdown across all indicators. Conclusions: There has been a marked change in trends of GI infections in the context of the COVID-19 pandemic. The drivers of this change are likely to be multifactorial; while changes in health seeking behaviour, pressure on diagnostic services and surveillance system ascertainment have undoubtably played a role there has likely been a true decrease in the incidence for some pathogens resulting from the control measures and restrictions implemented. This suggests that if some of these changes in behaviour such as improved hand hygiene were maintained, then we could potentially see sustained reductions in the burden of GI illness. • Our findings show that there has been a marked change in the burden of GI infections during the COVID-19 outbreak, and although undoubtably changes to health care and surveillance ascertainment have played a role, there does appear to be a true decrease in incidence. These findings suggest that if effective implementation of infection control measures were maintained, then we could see sustained reductions in the person to person transmission of GI illness in England. • This study was strengthened by the triangulation of data from several national and regional-based surveillance systems; using this approach we could determine that the trends observed were consistent across all indicators. • It has not been possible to definitively differentiate the relative contributions of the reduced ascertainment of GI infections versus a true decrease in GI disease burden in this study, which an additional focussed analysis could address. • This analysis includes only the first six-months of the COVID-19 outbreak response, and further longitudinal analyses will be performed to explore this further and assess any change as we move into further phases of the pandemic All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. The 2019 coronavirus pandemic has resulted in unparalleled challenges for society [1] . During 2020, the United Kingdom (UK) Government implemented a stepwise series of public health measures designed initially to contain, and then delay transmission of the virus (Figure 1 ). These measures ranged from public health information campaigns, rapid identification of cases and their contacts and isolation of those contacts in the initial phase of the outbreak (February to Mid-March 2020), with additional measures such as social distancing, education and business closures and enforceable 'lockdown' measures in the delay phase (Mid-March onwards; [2] ). Changes to healthcare provision and patient management were implemented concurrently to alleviate pressure on the National Health Service (NHS) and minimise nosocomial transmission of COVID-19 while continuing to provide essential care [2] . There is a growing body of evidence indicating that the COVID-19 pandemic and implemented control measures have had indirect impacts on other health conditions. Substantial decreases have been observed in emergency department (ED) attendances, with decreasing presentation of conditions such as strokes, surgical emergencies and cardiac emergencies, delays to cancer diagnoses, and concerns raised about delayed presentation and associated negative outcomes [3] [4] [5] [6] [7] . Less well documented are any indirect effects on communicable diseases, which are often controlled using similar nonpharmaceutical interventions to those implemented in the COVID-19 response [8] . Gastrointestinal (GI) infections are an important infectious cause of morbidity and mortality globally, placing a considerable burden on primary and secondary healthcare services. In England, it is estimated that there are in excess of 17 million cases annually, resulting in over 1 million healthcare consultations and around 90,000 confirmed laboratory diagnoses [9] [10] . Transmission of GI pathogens is typically faecal-oral, predominantly though consumption of contaminated food or water, or contact with infected individuals, animals or the contaminated environment and fomites; importance of transmission route varies substantially by pathogen. Control measures implemented during the COVID-19 response including improved hand hygiene, reduced social contact, increased environmental cleaning and closure of premises, all known to be effective in reducing GI infections, primarily those spread by person-to-person transmission and environmental contamination [8] . Using routinely collected surveillance data from several English surveillance systems coordinated by Public Health England (PHE), this study aimed to establish what impact the first six months of the COVID-19 outbreak response (27 January -2 August) have had on trends in GI infections. All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. A retrospective ecological study was conducted by performing secondary analyses on routinely collected national and regional surveillance data from eight national PHE coordinated surveillance systems, detailed in Table 1 , and Google Trend data. Systems included outbreak monitoring (HPzone), laboratory notifications Second Generation Surveillance System, (SGSS) and EpiNorth3, and real-time syndromic surveillance [11] [12] [13] . Syndromic systems covered the spectrum of severity ranging from the NHS 111 telephone health advice service and routine medical appointments captured in the general practitioner (GP) 'in hours' system (GPIH), to GP 'out of hours', which covers emergency GP appointments for acute or severe illness and the Emergency Department Syndromic Surveillance System (EDSSS), which captures those attending EDs [13]. Extracted data covering weeks 1 to 31 2020 (30 December 2019 -2 August 2020), and historic comparator data from weeks 1-31 2015-2019, was split into seven COVID-19 pandemic 'Phases' for comparison, determined by the key dates of UK governmental policy changes implemented during the COVID-19 response (Figure 1 ). These Phases comprised: Pre-outbreak (Phase 1); Early outbreak (Phase 2); Pre-lockdown (Phase 3); Early lockdown (Phase 4); Late lockdown (Phase 5); Lockdown easing (Phase 6); and Further easing (Phase 7; Table 2 ). Total weekly gastrointestinal outbreaks recorded in HPZone were determined for the seven Phases of 2020 and the 5-year average (2015-2019) with 95% confidence intervals calculated. HPZone data were further analysed by outbreak setting, PHE region and pathogen (including if the suspected pathogen was laboratory confirmed). Pseudonymised SGSS data for selected laboratory confirmed organisms (Campylobacter spp., Cryptosporidium spp., Shiga-toxin producing E. coli [STEC] , Giardia sp., Listeria spp., Norovirus, non-typhoidal Salmonella spp., Shigella spp.) were grouped by week of specimen sample date. Age group specific rates were calculated per 100,000 population using Office National Statistics 2019 England mid-year population estimates [14] . Cumulative regional and local authority rates per 100,000 population were determined for week 1 to 31 2020 and All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. ; https://doi.org/10.1101/2021.04.06.21254174 doi: medRxiv preprint the 5-year average for GI infections reported to SGSS for nine PHE regions (ranging from 2.6 -9.1 million population) and 150 local authority areas (average population size: 375,686). For geographies, risk ratios and percentage relative effects were calculated, and Pearson's correlation was performed for each local authority area using the cumulative COVID-19 rate per 100,000 population [15] . Syndromic data were analysed as described elsewhere [16] for data between week 1 and week 31 2020, with the same period in 2019 used as a comparator. Google Trend searches were performed for key phrases associated with GI illness in England, as described previously [17] . A score out of 100 is used to represent relative search interest over the given time period and geography. EpiNorth3 data were used to compare cases from Phases 2-7, 2020 to historic cases (2015-2019). A univariate case-case analysis was performed using exposure data, with cases reporting foreign travel excluded from analyses of other exposure categories. Comparisons were made between symptom presentation for historic and current cases. Time periods between onset date and specimen date and specimen date and referral date, and the duration of illness were determined, and a Mann-Whitney U test performed. Data from 2019 and 2020 were used to look at differences in laboratory diagnostic testing methods tests used, to account for the increasing use of molecular based techniques in recent years. All variables were plotted in a time series together with the weekly 5-year average and superimposed COVID-19 outbreak Phases, unless otherwise specified. Statistical analyses were performed using Stata software version 14.2. This study used routinely collected surveillance data. Patients were not involved in the development of the research question and outcome measures, the design of the study, the recruitment and conduct of the study. All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. ; https://doi.org/10.1101/2021.04.06.21254174 doi: medRxiv preprint During the first seven months of 2020, 1,544 suspected and laboratory-confirmed GI outbreaks were reported in England, representing a 52% decrease on the 5-year average for the period (3,208 (95% CI: 2,938 -3,478)). During the 'Pre-outbreak' (Phase 1; weeks 1-4), notified GI outbreaks were comparable to historic figures (Figure 1 and Table 1 ). Decreased reports were apparent from week 10 ('Pre-lockdown'; Phase 3; 11% decrease), with a low of 2,859 cases reported between weeks 13-18 ('Early lockdown'; Phase 4) representing a 66% decrease (5-year average: 8,345; (95% CI: 7,602-9,088)). Laboratory confirmed cases began to increase from week 16 onwards, mirroring the historic seasonal trend for reported GI pathogen activity despite numbers remaining significantly lower than average; during the historic peak for laboratory reporting, which occurred during lockdown easing, 4,617 cases were reported compared with the 5-year average of 7,879 (95% CI: 7,539-8,219); 41% decrease). While the total number of laboratory-confirmed cases was reduced, causative organisms were differently impacted when compared to the five-year average. Norovirus reports were most reduced (5.6% of all laboratory confirmed reports vs. 9.0%), with reductions also observed for Salmonella spp. (7.9% vs. 9.5%) and Cryptosporidium spp. (2.8% vs. 3.9%). The proportion of laboratory-confirmed cases with Giardia spp. (5.4% vs. 5.2%), STEC All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. ; https://doi.org/10.1101/2021.04.06.21254174 doi: medRxiv preprint Observed changes may reflect a real decrease in incidence or may be due to changes to healthcare provision or altered health-seeking behaviour or laboratory testing practices, resulting in reduced surveillance system ascertainment. ED attendances for gastroenteritis There was no difference in the time between onset date and specimen date for cases reported in Phase 2-Phase 7 2020, compared with historic cases (7 days IQR: 3-14 vs. 7 days (4-12 days); Wilcoxon rank sum p=0.600), with onset to specimen time comparable across the seven Phases of the COVID-19 outbreak. The time between specimen date and referral date and proportion of samples processed by culture (76.5% vs. 75.7%) and molecular techniques (17.2% vs. 15.5%) were also comparable. However, the proportion of specimens processed by light microscopy (protozoa) decreased (2.3% vs. 7.6%). The proportion of specimens submitted by general practitioners was 60.2% compared with 61.3% All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. vomiting (39% vs. 42%) were comparable, with an increase in cases reporting bloody diarrhoea in 2020 (24% vs. 16%). When comparing 2020 to historic cases, there was no difference in the duration of illness (7.5 days IQR: 5-12 vs. 8 days (6-12 days); Wilcoxon rank sum p=0.980), however as most cases are symptomatic when interviews are performed (~26% of current and historic cases), completion of this field is low. Using EpiNorth3 data it was possible to look at changes in exposures for cases of GI illness : 39-64) ). Outbreaks associated with food outlets also reduced significantly in Phase 3, prior to the lockdown period (3 vs. 13 (95% CI: 9-17)) and remained low until Phase 7 when pubs and restaurants reopened for dine-in customers (6 vs. 13 (95% CI: 9-17)). Outbreaks classified as 'other', All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. which included visitor attractions, were substantially decreased in Phase 4, when outbreaks associated with such settings are historically highest (7 vs. 51 (95% CI: 44-57)). Finally, evidence from Google Trends data showed searches for GI associated phrases such as 'Food poisoning', 'gastroenteritis' and 'sickness bug' all decreased dramatically between week 11 and week 13, while trends for 'handwashing' and 'disinfection' increased substantially between week 8 and week 14, mirroring decreases observed in other surveillance systems (Supplementary Figure 8 ). Analysis of routinely collected surveillance data from England's main laboratory, outbreak and syndromic surveillance systems showed marked changes in GI infection trends during the first six months of the COVID-19 outbreak response. Decreases in GI activity were observed across all surveillance indicators as restrictions were implemented in line with increasing COVID-19 activity [15] . As COVID-19 cases increased and further restrictions were implemented, health-seeking behaviour changed dramatically in England, with health service attendances decreasing from week 12 across all syndromic indictors [1, [18] [19] [20] [21] [22] . Similar decreases were observed internationally, with speculation that reduced healthcare usage was due to public avoidance, with some evidence that those with milder symptoms were least likely to seek care [3] [4] [5] [6] [7] 23 ]. However, behavioural surveys conducted during late lockdown and lockdown easing found 70-80% of participants had continued to seek care, if needed [24-25]. Protecting the health system was cited as a reason for healthcare avoidance by 16% of respondents with symptoms, while 10% of individuals reported difficulties in accessing their GP for physical complaints [24] [25] . In England, a government information campaign was launched from week 17 to encourage the public to continue to seek care, particularly for severe or acute conditions [2] ; however, our study shows that GI activity was increasing prior to this. Many syndromic indicators, such as those for noninfectious gastrointestinal conditions, rapidly returned to baseline levels during lockdown and easing, while gastrointestinal infections showed more modest increases [18] [19] [20] [21] . Behavioural studies undertaken during the first wave suggest good adherence to hygiene (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. ; https://doi.org/10.1101/2021.04.06.21254174 doi: medRxiv preprint higher during winter, with outbreaks predominantly associated with person-to-person transmission in health and social care settings; in the 2019/20 season, this outbreak activity appeared to have been partially curtailed by the COVID-19 response. Enhanced infection control measures were recommended in closed settings during week 8 [2] ; although there was evidence that measures were not being sufficiently implemented until later in the response [30] . Reports of outbreaks in food outlet and education settings were also reduced prior to closures announced as part of social distancing measures, and all surveillance indicators remained significantly lower than average despite the partial reopening of schools, restaurants and overseas travel corridors during the lockdown easing phase [2] . There was evidence that those pathogens spread predominantly by person-to-person transmission, such as norovirus and Shigella spp., showed greater reductions, while bacterial pathogens, which are more commonly foodborne and therefore less influenced by hygiene and social distancing measures, were least impacted [8, 31] . It is possible that those individuals with the most severe and prolonged infections, which tend to be bacterial, were more likely to access care, as seen with other diseases [4, 6, 8, 9] . However, a true decrease in activity was plausible given the measures implemented. Salmonella activity was likely substantially reduced by government guidance on non-essential foreign travel, in place from week 12 [2, 32] . Campylobacter, which is usually foodborne and often associated with incorrect food preparation was less impacted than other GI pathogens, although possible explanations for reductions may include food business closures and improved hygiene limiting the risk of cross-contamination. Cryptosporidiosis has strong seasonality with two peaks, one in late spring associated with C. parvum which occurs around lambing season and is often associated with petting farm outbreaks, which were closed as part of the COVID response, and the other, usually larger peak in late summer-early autumn mainly caused by C. hominis linked to increased recreational water use and foreign travel [33] . However, in 2020, C. hominis cases were virtually absent (Cryptosporidium Reference Unit data). It is likely that the closure of premises such as swimming pools and open farms have played a considerable role in this decline, and their reopening may impact on disease transmission. Reasons for the changes in the national picture observed for GI infections are likely to be complex and multifactorial, and it is not possible to attribute them to a specific cause. This study was strengthened by the triangulation of data from several surveillance systems; using this approach we could determine that the trends observed were consistent across all indicators. However, while this study has incorporated large national and regional-based surveillance systems, this is not comprehensive and there are other examples of operational GI surveillance systems which have not been included in this study. For example, the PHE All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. ; https://doi.org/10.1101/2021.04.06.21254174 doi: medRxiv preprint eFOSS system monitors foodborne and non-foodborne GI outbreaks across England, however, due to a small number of outbreaks reported by the system it was felt that these data were not sufficiently powered to add to the overall findings of the study [34] . There are further limitations to this work; it has not been possible to definitively differentiate the relative contributions of the reduced ascertainment of GI infections versus a true decrease in GI disease burden in this study, which an additional focussed analysis could address. An additional limitation of this study is that negative results are not captured by the SGSS laboratory surveillance system, therefore it was not possible to determine to what degree the changes were due to changes in testing. We were not able to calculate the positivity rate to assess whether only severe cases were being tested, although evidence from the North East suggested that symptomatology was comparable between 2020 cases and historic cases. Guidance was released in week 13 recommending the cessation of routine culture for nonbloody diarrhoea might be considered if laboratories were struggling to deliver the service [35] . However, by then laboratory confirmed cases were beginning to increase again, while other contemporaneous changes implemented to GI laboratory testing methods, such as the introduction of molecular methods could differentially affect ascertainment of GI pathogens. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. This analysis includes only the first six-months of the COVID-19 outbreak response, and further longitudinal analyses will be performed to explore this further and assess any change as we move into further phases of the pandemic including the relaxation of social distancing measures, further lockdown measures, and the usual winter outbreak period. All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. Pubs and restaurants reopen f or dine-in customers (04/07/2020) All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. ; Week 1 and Week 31 2020 and the 5-year weekly average (95% confidence interval), by COVID -19 outbreak Phase and age group a b c d e f All rights reserved. No reuse allowed without permission. (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. The copyright holder for this preprint this version posted April 7, 2021. ; https://doi.org/10.1101/2021.04.06.21254174 doi: medRxiv preprint The COVID-19 pandemic: a new challenge for syndromic surveillance Covid-19 policy tracker: a timeline of national policy and health system responses to covid-19 in England Impact of COVID-19 outbreak on emergency surgery and emergency department admissions: an Italian level 2 emergency department experience What has caused the fall in stroke admissions during the COVID-19 pandemic? Impact of COVID-19 pandemic on acute spine surgery referrals to UK tertiary spinal unit: any lessons to be learnt? Emergency department use during COVID-19 as described by syndromic surveillance Collateral damage: Medical care avoidance behavior among patients with myocardial infarction during the COVID-19 pandemic. JACC: Case Reports Communicable Disease. Control Handbook. Second Edition Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice Routine reports of gastrointestinal infections in humans, England and Wales. Health Protection The development and deployment of a national web-based system for communicable disease control in England Estimates of the population for the Weekly COVID-19 surveillance report Assessing the Likely Impact of a Rotavirus Vaccination Program in England: The Contribution of Syndromic Surveillance Temporal Relationship Between Healthcare-Associated and Nonhealthcare-Associated Norovirus Outbreaks and Google Trends Data in the United States Remote Health Advice Syndromic Surveillance System weekly report GP In Hours Syndromic Surveillance System weekly report GP Out of Hours Syndromic Surveillance System weekly report Emergency Department Syndromic Surveillance System weekly report The authors acknowledge the contribution and support from all data providers including:NHS 111 and NHS Digital; QSurveillance®, University of Oxford, EMIS/EMIS practices, ClinRisk®, TPP, ResearchOne and participating SystmOne GP practices; Advanced and the participating OOH service providers; participating EDSSS emergency departments, Royal Routine laboratory notif ications f rom NHS laboratories including statutory notif ications of laboratory conf irmed notif iable organisms.