Elsevier

Journal of Hazardous Materials

Volume 296, 15 October 2015, Pages 30-36
Journal of Hazardous Materials

Fate of Escherichia coli O157: H7 in agricultural soils amended with different organic fertilizers

https://doi.org/10.1016/j.jhazmat.2015.04.023Get rights and content

Highlights

  • Escherichia coli O157:H7 survival time (td) prolonged as a result of organic fertilizers application, especially in acidic soils.

  • Shorter td values were observed in soils amended with chicken manure and the longest in soils amended with pig manure.

  • The td values are longer in original soils with higher pH and lower free Fe2O3.

  • Electrical conductivity played a more important role in regulating E. coli O157:H7 survival in fertilizer-amended soils.

Abstract

Five organic fertilizers (vermicompost, pig manure, chicken manure, peat and oil residue) were applied to agricultural soils to study their effects on the survival of Escherichia coli O157:H7 (E. coli O157:H7). Results showed that E. coli O157:H7 survival changed greatly after organic fertilizers application, with shorter td values (survival time needed to reach the detection limit of 100 CFU g−1) (12.57 ± 6.57 days) in soils amended with chicken manure and the longest (25.65 ± 7.12 days) in soils amended with pig manure. Soil pH, EC and free Fe/Al (hydro) oxides were significant explanatory factors for E. coli O157:H7 survival in the original soils. Soil constituents (minerals and organic matter) and changes in their surface charges with pH increased the effect of soil pH on E. coli O157:H7 survival. However, electrical conductivity played a more important role in regulating E. coli O157:H7 survival in fertilizer-amended soils. This study highlighted the importance of choosing appropriate organic fertilizers in the preharvest environment to reduce food-borne bacterial contamination.

Introduction

During the past decade, outbreaks of food-borne illnesses associated with the consumption of contaminated food produce continue to be a public health problem. Fresh produce can be contaminated with various human pathogens including bacteria, protozoa and viruses. Among the bacterial pathogens, numerous outbreaks are caused by Escherichia coli O157:H7 (E. coli O157:H7), which is dangerous because of its low infective dose (as few as 10 cells), high pathogenicity and ability to survive under frozen conditions [1]. Moreover, the virulence genes were found to be transferable to non-pathogenic E. coli strains [2]. In China, the first E. coli O157:H7 strain was isolated from hemorrhagic colitis patients in Xuzhou city, Jiangsu Province in 1986. No recognized outbreak has yet been reported. But several sporadic cases of E. coli O157:H7 infections have been detected in many different provinces [3], [4].

Raw fruits and vegetables, especially fresh-cut leafy greens, are increasingly being recognized as the foremost transmitting vehicles of E. coli O157:H7 [5]. Although, fresh produce can be contaminated at any point along the farm-to-consumption handling chain, the field application of raw manure or contaminated irrigation water in the primary production phase is a principal route of E. coli O157:H7 contamination [6], [7], [8]. Hence, it is critical to prevent fresh produce from preharvest contamination in order to achieve the delivery of microbiologically safe produce to consumers [5]. Knowledge of the behavior of E. coli O157:H7 in plants growing in substrates like soil is important to develop strategies for minimizing contamination.

Depending on the soil properties and environmental factors, the reported survival times of E. coli O157:H7 in soil ranges from several days to more than 6 months [6], [7], [8], [9], [10]. The availability of resources, such as carbon substrates, is probably a principal factor that affects the persistence of E. coli O157:H7 in natural environments, such as soil and water [6]. Utilization of organic materials (e.g., farmyard manure and slurry) is the most economic and practical option for improving soil quality while also providing additional sources of nutrients for growing plants [8]. Approximately 1011 ton of agricultural animal manure are produced globally each year and routinely applied to the soil as a crop fertilizer [11]. However, the application of organic materials could increase the incidence of disease caused by soil-borne fungal pathogens [12], [13]. Likewise, the application of organic fertilizer may also influence the survival capacity of E. coli O157:H7 in soils [8], [14]. For instance, Unc and Goss [14] reported that E. coli survived longer in soils amended with swine manure. Currently, most reports are concerned with animal manures and/or slurries [6], [8], [14]. Fertilizers such as peat and oil residue, are main organic fertilizers used worldwide. Little is known about the effect of other kinds of organic fertilizers on the survival of human enteric pathogens in agricultural soils.

In the present study, soils from vegetable fields with various physico-chemical properties were collected to study how E. coli O157:H7 survival is affected by the application of different organic fertilizers. More specifically, the goals were to: (i) investigate the factors regulating E. coli O157:H7 survival in soils, (ii) identify the effect of different fertilizer-amended soil characteristics which are responsible for differences in E. coli O157:H7 survival, and (iii) assess the possible risk of E. coli O157:H7 contamination when soil is amended with organic fertilizer.

Section snippets

Organic fertilizers and soils

Five types of organic fertilizers (vermicompost, pig manure, chicken manure, peat and oil residue) which have various properties, were used in this study (Table 1). Pig manure was obtained from a commercial pig farm and air-dried. The other organic fertilizers were produced commercially by the same company. Four soils (P, H, N and E) of surface horizon (0–20 cm) were collected from vegetable fields in eastern China (P, 29.036°N, 119.452°E, Plinthudult; H, 30.349°N, 120.202°E, Hapludult; N,

Survival parameters for E. coli O157:H7 in soils

Enumeration analysis detected no E. coli O157:H7 in the non-inoculated soil samples throughout the entire incubation period. Changes in E. coli O157:H7 counts with time in the test soils are shown in Fig. 1. To compare the survival kinetics of the test soils, the survival data were fitted to the Weibull model. The Weibull model can fit the experimental data very well with a mean R2 of 0.97. Moreover, variations in model parameters were observed in different soils, especially the δ values that

Discussion

We assessed the effect of organic fertilizer on the survival of a key bacterial pathogen, E. coli O157:H7 in agricultural soils with various physicochemical properties. With the same incubation temperature and moisture, the survival of E. coli O157:H7 varied in soils as a result of organic fertilizer amendment. The Weibull model proved to be a suitable model for describing the decline of E. coli O157:H7 in the test soils. Even though the Weibull model is an empirical model, it can be linked to

Conclusions

This research revealed the effects of organic fertilizers application on E. coli O157:H7 survival in agricultural soils. Soil pH, EC and Fe/Al (hydro) oxides were important factors controlling the E. coli O157:H7 survival in original soils without fertilizer amendment. With fertilizer-amended soils, soil EC, pH, WSOC and NO3-N content were the most important regulating factors, with EC as the most important one. Organic fertilizer application, particularly pig manure, showed great positive

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 40971255). We thank Professor Philip C. Brookes from Rothamsted Research, UK for helping to edit the manuscript.

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