Re-shaping models to forecast faecal pathogen risk to humans

Lead Research Organisation: University of Stirling
Department Name: Biological and Environmental Sciences


Since the early 20th century simple approaches (termed 1st-order kinetics) have been used to describe the population decline of bacteria in research fields as diverse as medicine, food biotechnology and environmental microbiology. When used to describe populations of faecal bacteria and pathogens in livestock faeces, these kinetics are commonly referred to as 'die-off', reflecting the generally held view that populations decline after faeces has been deposited. Consequently any potential risk of transfers to the wider environment and humans is thought to lessen with the passing of time after faeces deposition and thus models and policies reflect this. However, this project will combine new data with modelling to show that describing population change dynamics in terms of a 1st-order decline is flawed because of it failing to account for population increases that occur under fluctuating environmental conditions. This will reveal a major underestimation of diffuse source bacterial risks from cattle to soil and water quality, with increased threats to public health that may worsen if combined with expected climate change outcomes.

Knowledge of microbial dynamics is partial in the sense that much work has focused on controlled laboratory experiments. Field relevant die-off profiles need to incorporate the interaction of a suite of climatic drivers thought to impact on microbial persistence (e.g. temperature, UV, episodic rewetting). New research under field conditions has speculated that bacterial growth in faecal material may be a significant factor for protracting bacterial persistence once outside the animal host. However, a key limitation of such studies is the analysis of only a few faecal samples during the immediate period post defecation. Higher resolution sampling is imperative to understand growth potential better. Our aim is to 'reshape' the credibility of modelled faecal bacteria population dynamics to ensure they reflect a more appropriate representation of growth within the mathematical profiling of bacterial persistence. The project focuses on cattle faeces as an example and quantifies the extent of error between the two approaches of accounting for, or ignoring, bacteria growth when calculating budgets of faecal bacteria deposited on pasture.

The project draws on data provided by replicated field experiments. This empirical data underpins the development of the model to account for bacterial growth in dairy faeces. Our approach derives seasonal population change profiles for E. coli (a key faecal indicator organism) by collecting 16 time-series samples per seasonal experiment. Eight of these samples are collected at high resolution within the first 10 days of the experiment, including two samples collected at half day intervals on day 0. This represents a marked change from previous low frequency sampling regimes. We include a critical examination of modelled approximations of bacterial die-off using different hypothetical farm scenarios to evaluate the cumulative implications of the revised 'die-off' pattern on bacterial budgets on pasture. To facilitate this we use an existing empirical model (assuming 1st-order 'die-off' and livestock excretion rates) and amend the existing model code to reflect growth as observed through the field experiments. The output represents one of the first attempts to quantify the degree of error associated with assumptions of 1st-order decline using field relevant data and will set a precedent for acknowledging the potential under- or over- estimation of terrestrial faecal bacteria reservoirs contributed to by grazing cattle. The project assesses two main issues: (1) the magnitude of population increase of faecally derived bacteria within faeces on pasture through contrasting seasons; and (ii) the degree of under- or over- estimation of faecal bacteria burden to land if the population increase phase is ignored in modelled approximations of microbial decline.

Planned Impact

Outside of academia this research will benefit several central government departments and agencies, most specifically the Scottish Environment Protection Agency, Environment Agency, and Defra, and will be of use to water utilities too. Faecal bacteria are key parameters monitored within the revised Bathing Waters Directive and Shellfisheries Directive to regulate EU compliance of microbial water quality. Thus, understanding and appreciating the potential source loadings of faecal bacteria from livestock is important to those who work in areas of research and business linked to these Directives. Ultimately this work seeks to improve quality of life for those enjoying recreational activities in rural environments. For example bathing and surfing at designated coastal waters, and camping on land previously used as pasture. However, the value of scientific advice to policy makers and regulators can be compromised by the gap in the study scale at which scientists typically investigate processes versus the complexity of the real world. The over reliance on laboratory scale studies of pathogen indicator persistence is a clear example of this whereby real world scenarios are mis-represented through the use of laboratory data collected under controlled conditions. Policy makers and regulators will gain immediately from these findings to help improve current modelling approaches for determining, as cannot now be done, accurate source burden of faecal microbes on land based on actual survival patterns rather than crude approximations. It is paramount that we strive to understand the complexity of pathogen indicator population behavior (see support from the SEPA Environmental Quality Unit Manager).

In 2010 only just over half (418 out of 769 tested) of UK bathing beaches were recommended by the Marine Conservation Society (MCS) for excellent water quality. Over the past 3 years, since a peak in the number of MCS recommended beaches in 2006 and 2007, water quality has declined. Today, poor water quality is often linked with heavy rainfall and recent wetter summers have made this type of pollution worse. MCS is concerned that the current situation may further deteriorate when new stricter bathing water standards are introduced in 2015 under the 'revised Bathing Water Directive'. Under this new regime approximately 14% of Britain's beaches are at risk of failing the new minimum water quality standard if nothing's done to improve them. The MCS would therefore welcome the proposed research which would help to inform bathing water improvement plans and highlight the need to reduce polluting runoff from farmland with the introduction of better farm management practices(see support).

The PI is well-placed to ensure that research findings are disseminated with highest impact given his existing links to Defra and other bodies. The PI has been engaged with all principal UK regulators and policy makers and has links to those with a specific responsibility for facilitating KE within a diffuse pollution work-package in a NERC KE grant: the Catchment Change Network (see Haygarth letter of support). Research findings will therefore be channeled through appropriate networks and science user communities to promote better understanding and management of uncertainty and risk linked to land and water related issues.

The project will proactively promote public understanding of science. The PI has identified a 'Café Scientifique' discussion forum running in Edinburgh. It is believed that this will provide a key opportunity for debating science issues and importantly will promote public engagement with science. This means of engagement is much more informal and accessible than a public lecture and will be open to audiences of people who are interested in science but generally do not have the opportunity to engage and discuss their views. Stakeholders, including SEPA, MCS and Surfers against Sewage will also attend to stimulate debate (see support).
Description E. coli and coliform persistence profiles in dairy faeces under field relevant conditions were derived for Spring, Summer, Autumn and Winter in 2012 & 2013 in Scotland. Contrasting profiles have also been derived in faecal material protected from rainfall and exposed to warmer and more humid conditions. Seasonal & year-on-year variability in E. coli persistence profiles in this faecal matrix was explored.

The research spanned two consecutive years to provide a repeat of four seasonal experiments. The rationale was to assess the potential for year-on-year variability in E. coli regrowth and die-off because of shifts in seasonal climatic variables such as temperature and rainfall. The repeat of the seasonal experiment proved valuable as the two year period of study has so far captured some contrasting environmental conditions. Spring 2012 included an unseasonably hot week-long period followed by freezing conditions (a drop in temperature of 27oC). In contrast spring 2013 was extremely cold and wintery, with March 2013 being one of the coldest on record in the UK, and was preceded by the 2nd wettest UK summer ever recorded. Interestingly, a milder spell during mid-April 2013 saw dramatic increases in E. coli CFUs, particularly in faecal material protected from rainfall and exposed to more humid conditions - clear signals of the role of warmth in promoting cell persistence.

In addition to the derivation of a series of persistence profiles, the project contributed to a record of seasonal, inter-annual and within-herd variability of E. coli concentrations in freshly deposited dairy faeces for central Scotland. Findings from this phase of the study have now been published (see publications tab).

A cross comparison study exploring the persistence profiles of E. coli in dairy faeces as determined by culture and molecular-based approaches has also been undertaken. Cell counts observed using selective media were recorded in parallel with outputs derived by quantitative polymerase chain reaction (qPCR). This paper is now published in Environmental Science & Technology, and an additional paper documenting the entire dataset from the two year experiment under all treatment conditions was published in Scientific Reports.
Exploitation Route The data are being used to refine an empirical model that predicts the burden of E. coli on grazed pasture. The regrowth profiles are being embedded into the model code. Subsequent funding has been secured to develop a decision support tool for farm advisors (see
Sectors Agriculture, Food and Drink,Environment

Description Data generated in this project was used to develop a practical tool to enable the visualisation of FIO source risks in agricultural environments and so demonstrate more effective land management to reduce diffuse microbial pollution. The data helped to underpin the 'Visualising Pathogen & Environmental Risk' innovation project.
First Year Of Impact 2015
Sector Agriculture, Food and Drink,Environment
Impact Types Policy & public services

Description Presentation at 2014 13th IWA Specialized Conference on Watershed and River Basin Management 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Discussion and networking with interested academics regarding future research opportunities.

discussion surrounding next steps for research and potential links
Year(s) Of Engagement Activity 2014
Description Testing the waters: understanding microbial pollution at the beach 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact A team from the wider 'Delivering Healthy Water' project ran a public engagement event via the Café Scientifique forum in February 2013. David Oliver, Richard Quilliam, Andy Cummins and Jonathan Porter discussed bathing water quality with an audience of 60 café-goers at the Phoenix Bar in Exeter.

Exeter was chosen as the venue given its longstanding hosting of café Scientifique events and because over a quarter of bathing waters in England are located in the South West and livestock farming is a dominant agricultural sector in this region.

The evening provided a chance to share information and research findings to members of the public. It also served as an opportunity to capture the views of those interested in the subject area and answer questions on bathing water quality and information.

Increased public understanding of bathing water quality and testing
Year(s) Of Engagement Activity 2013