Modeling on-farm Escherichia coli O157:H7 population dynamics

Abstract

Escherichia coli O157:H7 is a potentially fatal foodborne pathogen with a putative reservoir for human infection in feedlot cattle. In order to more effectively identify targets for intervention strategies, we aimed to (1) assess the role of various feedlot habitats in E. coli O157:H7 propagation and (2) provide a framework for examining the relative contributions of animals and the surrounding environment to observed pathogen dynamics. To meet these goals we developed a mathematical model based on an ecological metapopulation framework to track bacterial population dynamics inside and outside the host. We used E. coli O157:H7 microbiological and epidemiological literature to characterize E. coli O157:H7 habitats at the pen level and account for E. coli O157:H7 population processes in water troughs, feedbunks, cattle hosts, and pen floors in the model. Simulations indicated that E. coli O157:H7 was capable of maintaining viable populations in the feedlot without net growth in the cattle gastrointestinal tract, suggesting E. coli O157:H7 may not always act as an obligate parasite. Water troughs and contaminated pen floors appeared to be particularly influential sources driving E. coli O157:H7 population dynamics and thus would serve as prime environmental targets for interventions to effectively reduce the E. coli O157:H7 load at the pen level.

FIG. 1.

Diagrammatic representation of model states and flows. Boxes represent patches where E. coli O157:H7 can reside. Arrows represent migration rates between patches with flow from patch i to patch j represented by m_ij. Large arrows indicate density-dependent exponential growth of bacteria within each patch.

FIG. 2.

The number of E. coli O157:H7 colony-forming units (CFU; log10) observed in each patch (left panel) and the number of log10 CFU per gram of substrate in each patch (right panel).

FIG. 3.

Each panel is the bifurcation diagram of the respective patch comparing the growth rate and log carrying capacity per gram (K) with the effect on the number of colony-forming units (CFU) of E. coli O157:H7 per gram of fecal matter (note change in x-axis between panels). Changes in water parameters have little effect on the shedding dynamics, while changes in parameters of other patches do have substantial influence at values examined here.

FIG. 4.

Steady state solutions for proportion of E. coli O157:H7 population in each patch with different capacities of water trough in liters.

FIG. 5.

Effect of varying the number of steers (S) in a pen and the capacity of the water trough (L) on the log10 colony-forming units (CFU) of E. coli O157:H7 observed per gram of fecal matter. Two clear planes emerge with a bifurcation resulting as the number of steers is decreased or capacity of water troughs increased.

FIG. 6.

A quantile box plot (left panel) and frequency histogram (right panel) of log colony-forming units (CFU) of E. coli O157:H7 per gram of fecal matter at equilibrium in stochastic simulations. The dotted line in both panels (horizontal on left and vertical on right) represents the minimum level of reliable detection in culture with immunomagnetic bead separation, the method most often used to test fecal samples for E. coli O157:H7.

FIG. 7.

Spearman's correlation (ρ) values indicating strength of the relationship between parameter and model output (colony-forming units [CFU] of E. coli O157:H7 per gram of feces at equilibrium) as determined by stochastic simulations. Only parameters with statistically significant correlations are shown.