A Predictive Model for Survival of Escherichia coli O157:H7 and Generic E. coli in Soil Amended with Untreated Animal Manure

This study aimed at developing a predictive model that captures the influences of a variety of agricultural and environmental variables and is able to predict the concentrations of enteric bacteria in soil amended with untreated Biological Soil Amendments of Animal Origin (BSAAO) under dynamic conditions. We developed and validated a Random Forest model using data from a longitudinal field study conducted in mid‐Atlantic United States investigating the survival of Escherichia coli O157:H7 and generic E. coli in soils amended with untreated dairy manure, horse manure, or poultry litter. Amendment type, days of rain since the previous sampling day, and soil moisture content were identified as the most influential agricultural and environmental variables impacting concentrations of viable E. coli O157:H7 and generic E. coli recovered from amended soils. Our model results also indicated that E. coli O157:H7 and generic E. coli declined at similar rates in amended soils under dynamic field conditions.The Random Forest model accurately predicted changes in viable E. coli concentrations over time under different agricultural and environmental conditions. Our model also accurately characterized the variability of E. coli concentration in amended soil over time by providing upper and lower prediction bound estimates. Cross‐validation results indicated that our model can be potentially generalized to other geographic regions and incorporated into a risk assessment for evaluating the risks associated with application of untreated BSAAO. Our model can be validated for other regions and predictive performance also can be enhanced when data sets from additional geographic regions become available.

[1]  E. Atwill,et al.  Environmental inactivation and irrigation-mediated regrowth of Escherichia coli O157:H7 on romaine lettuce when inoculated in a fecal slurry matrix , 2019, PeerJ.

[2]  P. Millner,et al.  Survival of Escherichia coli in Manure-Amended Soils Is Affected by Spatiotemporal, Agricultural, and Weather Factors in the Mid-Atlantic United States , 2018, Applied and Environmental Microbiology.

[3]  R. Baker,et al.  Mechanistic models versus machine learning, a fight worth fighting for the biological community? , 2018, Biology Letters.

[4]  A. Pradhan,et al.  Evaluation of meteorological factors associated with pre-harvest contamination risk of generic Escherichia coli in a mixed produce and dairy farm , 2018 .

[5]  A. Mishra,et al.  Identifying and modeling meteorological risk factors associated with pre-harvest contamination of Listeria species in a mixed produce and dairy farm. , 2017, Food research international.

[6]  Zachary M. Jones,et al.  edarf: Exploratory Data Analysis using Random Forests , 2016, J. Open Source Softw..

[7]  P. Millner,et al.  Survival and Persistence of Nonpathogenic Escherichia coli and Attenuated Escherichia coli O157:H7 in Soils Amended with Animal Manure in a Greenhouse Environment. , 2016, Journal of food protection.

[8]  Y. Pachepsky,et al.  Survival of Manure-borne and Fecal Coliforms in Soil: Temperature Dependence as Affected by Site-Specific Factors. , 2016, Journal of environmental quality.

[9]  P. Fravalo,et al.  Persistence of Indicator and Pathogenic Microorganisms in Broccoli following Manure Spreading and Irrigation with Fecally Contaminated Water: Field Experiment. , 2015, Journal of food protection.

[10]  K. Meyer,et al.  Modeling microbial growth and dynamics , 2015, Applied Microbiology and Biotechnology.

[11]  M. Wiedmann,et al.  Spatial and Temporal Factors Associated with an Increased Prevalence of Listeria monocytogenes in Spinach Fields in New York State , 2015, Applied and Environmental Microbiology.

[12]  M. Uyttendaele,et al.  Persistence of Pathogenic and Non-Pathogenic Escherichia coli Strains in Various Tropical Agricultural Soils of India , 2015, PloS one.

[13]  J. Lejeune,et al.  Soil Conditions That Can Alter Natural Suppression of Escherichia coli O157:H7 in Ohio Specialty Crop Soils , 2015, Applied and Environmental Microbiology.

[14]  Amirhossein Mokhtari,et al.  Transfer of Escherichia coli O157:H7 from simulated wildlife scat onto romaine lettuce during foliar irrigation. , 2015, Journal of food protection.

[15]  M. Ellouze,et al.  Extending the gamma concept to non-thermal inactivation: a dynamic model to predict the fate of Salmonella during the dried sausages process. , 2015, Food microbiology.

[16]  M. Jun,et al.  Multifactorial Effects of Ambient Temperature, Precipitation, Farm Management, and Environmental Factors Determine the Level of Generic Escherichia coli Contamination on Preharvested Spinach , 2015, Applied and Environmental Microbiology.

[17]  Matt Golder,et al.  Big Data, Causal Inference, and Formal Theory: Contradictory Trends in Political Science? , 2014, PS: Political Science & Politics.

[18]  D. Crowley,et al.  Persistence of Escherichia coli O157 and non-O157 strains in agricultural soils. , 2014, The Science of the total environment.

[19]  J. Schijven,et al.  Meta-regression analysis of commensal and pathogenic Escherichia coli survival in soil and water. , 2014, Environmental science & technology.

[20]  A. Geeraerd,et al.  Modeling the fate of Escherichia coli O157:H7 and Salmonella enterica in the agricultural environment: current perspective. , 2014, Journal of food science.

[21]  M. Doyle,et al.  Examination of factors for use as potential predictors of human enteric pathogen survival in soil , 2014, Journal of applied microbiology.

[22]  Laosheng Wu,et al.  Survival of Escherichia coli O157:H7 in Soils from Jiangsu Province, China , 2013, PloS one.

[23]  J. Frank,et al.  Modeling the influence of temperature, water activity and water mobility on the persistence of Salmonella in low-moisture foods. , 2013, International journal of food microbiology.

[24]  S. Tyrrel,et al.  IMPACT OF SOIL TYPE, BIOLOGY AND TEMPERATURE ON THE SURVIVAL OF NON-TOXIGENIC ESCHERICHIA COLI O157 , 2013, Biology and Environment: Proceedings of the Royal Irish Academy.

[25]  Laosheng Wu,et al.  Survival of Escherichia coli O157:H7 in Soils from Vegetable Fields with Different Cultivation Patterns , 2013, Applied and Environmental Microbiology.

[26]  M. Wiedmann,et al.  Landscape and Meteorological Factors Affecting Prevalence of Three Food-Borne Pathogens in Fruit and Vegetable Farms , 2012, Applied and Environmental Microbiology.

[27]  J. Cevallos-Cevallos,et al.  Adhesion and splash dispersal of Salmonella enterica Typhimurium on tomato leaflets: effects of rdar morphotype and trichome density. , 2012, International journal of food microbiology.

[28]  D. Crowley,et al.  Persistence of Escherichia coli O157:H7 in major leafy green producing soils. , 2012, Environmental science & technology.

[29]  M. Gilmour,et al.  Comparative examination of Escherichia coli O157:H7 survival on romaine lettuce and in soil at two independent experimental sites. , 2012, Journal of food protection.

[30]  J. Cevallos-Cevallos,et al.  Dispersal of Salmonella Typhimurium by rain splash onto tomato plants. , 2012, Journal of food protection.

[31]  E. Franz,et al.  Variability of Escherichia coli O157 Strain Survival in Manure-Amended Soil in Relation to Strain Origin, Virulence Profile, and Carbon Nutrition Profile , 2011, Applied and Environmental Microbiology.

[32]  M. Peleg,et al.  Microbial Growth Curves: What the Models Tell Us and What They Cannot , 2011, Critical reviews in food science and nutrition.

[33]  D. Crowley,et al.  Persistence of Escherichia coli O157:H7 and Its Mutants in Soils , 2011, PloS one.

[34]  D. Makowski,et al.  Predicting invasion success of forest pathogenic fungi from species traits , 2011 .

[35]  Orin C. Shanks,et al.  Decay of Bacterial Pathogens, Fecal Indicators, and Real-Time Quantitative PCR Genetic Markers in Manure-Amended Soils , 2011, Applied and Environmental Microbiology.

[36]  C. Muyanja,et al.  Survival of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in manure and manure‐amended soil under tropical climatic conditions in Sub‐Saharan Africa , 2011, Journal of applied microbiology.

[37]  C. Muyanja,et al.  Kinetic model‐based prediction of the persistence of Salmonella enterica serovar Typhimurium under tropical agricultural field conditions , 2011, Journal of applied microbiology.

[38]  J. Trevors,et al.  Survival of Escherichia coli in the environment: fundamental and public health aspects , 2011, The ISME Journal.

[39]  C. Muyanja,et al.  Transfer and internalisation of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in cabbage cultivated on contaminated manure-amended soil under tropical field conditions in Sub-Saharan Africa. , 2011, International journal of food microbiology.

[40]  B. Vinnerås,et al.  Inactivation of Escherichia coli O157:H7 and Salmonella Typhimurium in manure-amended soils studied in outdoor lysimeters , 2010 .

[41]  Jean-Michel Poggi,et al.  Variable selection using random forests , 2010, Pattern Recognit. Lett..

[42]  A. V. Bruggen,et al.  COLIWAVE a simulation model for survival of E. coli O157:H7 in dairy manure and manure-amended soil , 2010 .

[43]  T. Oscar General regression neural network and monte carlo simulation model for survival and growth of salmonella on raw chicken skin as a function of serotype, temperature, and time for use in risk assessment. , 2009, Journal of food protection.

[44]  A. V. Van Bruggen,et al.  Estimating the stability of Escherichia coli O157:H7 survival in manure-amended soils with different management histories. , 2008, Environmental microbiology.

[45]  A. V. Van Bruggen,et al.  Manure-amended soil characteristics affecting the survival of E. coli O157:H7 in 36 Dutch soils. , 2008, Environmental microbiology.

[46]  C. Prigent-Combaret,et al.  Persistence of Shiga toxin‐producing Escherichia coli O26 in various manure‐amended soil types , 2007, Journal of applied microbiology.

[47]  D. Korber,et al.  Effect of soil composition, temperature, indigenous microflora, and environmental conditions on the survival of Escherichia coli O157:H7. , 2007, Canadian journal of microbiology.

[48]  Z. Dou,et al.  Survival of Salmonella enterica Serovar Newport in Manure and Manure-Amended Soils , 2006, Applied and Environmental Microbiology.

[49]  A. Prasad,et al.  Newer Classification and Regression Tree Techniques: Bagging and Random Forests for Ecological Prediction , 2006, Ecosystems.

[50]  Thomas E Oscar,et al.  Validation of Lag Time and Growth Rate Models for Salmonella Typhimurium: Acceptable Prediction Zone Method , 2005 .

[51]  David L. Jones,et al.  Escherichia coli O157 survival following the surface and sub-surface application of human pathogen contaminated organic waste to soil , 2004 .

[52]  M. Doyle,et al.  Fate of Escherichia coli O157:H7 in Manure-Amended Soil , 2002, Applied and Environmental Microbiology.

[53]  J Olley,et al.  Predictive microbiology: towards the interface and beyond. , 2002, International journal of food microbiology.

[54]  J. Friedman Greedy function approximation: A gradient boosting machine. , 2001 .

[55]  J. Verhaegen,et al.  Survival of E. coli and Enterococcus spp. derived from pig slurry in soils of different texture , 2001 .

[56]  Mark S. Coyne,et al.  Mortality of Escherichia coli O157: H7 in two soils with different physical and chemical properties. , 2000 .

[57]  D. Bolton,et al.  The‐survival‐characteristics‐of‐a‐non‐toxigenic‐strain‐of‐Escherichia‐coli‐O157:H7 , 1999, Journal of applied microbiology.

[58]  J Olley,et al.  Relationship between temperature and growth rate of bacterial cultures , 1982, Journal of bacteriology.

[59]  Laosheng Wu,et al.  Survival of Escherichia coli O157:H7 in soils under different land use types , 2013, Environmental Science and Pollution Research.

[60]  Organización Mundial de la Salud Microbiological hazards in fresh leafy vegetables and herbs: meeting report , 2008 .

[61]  Andy Liaw,et al.  Classification and Regression by randomForest , 2007 .

[62]  B. Chambers,et al.  Pathogen survival during livestock manure storage and following land application. , 2005, Bioresource technology.

[63]  L. Breiman Random Forests , 2001, Machine Learning.