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. 2018 Oct 16:9:2451.
doi: 10.3389/fmicb.2018.02451. eCollection 2018.

Agricultural Practices Influence Salmonella Contamination and Survival in Pre-harvest Tomato Production

Ganyu Gu  1 , Laura K Strawn  1 , David O Oryang  2 , Jie Zheng  2 , Elizabeth A Reed  2 , Andrea R Ottesen  2 , Rebecca L Bell  2 , Yuhuan Chen  2 , Steven Duret  2 , David T Ingram  2 , Mark S Reiter  1 , Rachel Pfuntner  1 , Eric W Brown  2 , Steven L Rideout  1
Affiliations

Agricultural Practices Influence Salmonella Contamination and Survival in Pre-harvest Tomato Production

Ganyu Gu et al. Front Microbiol. .

Abstract

Between 2000 and 2010 the Eastern Shore of Virginia was implicated in four Salmonella outbreaks associated with tomato. Therefore, a multi-year study (2012-2015) was performed to investigate presumptive factors associated with the contamination of Salmonella within tomato fields at Virginia Tech's Eastern Shore Agricultural Research and Extension Center. Factors including irrigation water sources (pond and well), type of soil amendment: fresh poultry litter (PL), PL ash, and a conventional fertilizer (triple superphosphate - TSP), and production practices: staked with plastic mulch (SP), staked without plastic mulch (SW), and non-staked without plastic mulch (NW), were evaluated by split-plot or complete-block design. All field experiments relied on naturally occurring Salmonella contamination, except one follow up experiment (worst-case scenario) which examined the potential for contamination in tomato fruits when Salmonella was applied through drip irrigation. Samples were collected from pond and well water; PL, PL ash, and TSP; and the rhizosphere, leaves, and fruits of tomato plants. Salmonella was quantified using a most probable number method and contamination ratios were calculated for each treatment. Salmonella serovar was determined by molecular serotyping. Salmonella populations varied significantly by year; however, similar trends were evident each year. Findings showed use of untreated pond water and raw PL amendment increased the likelihood of Salmonella detection in tomato plots. Salmonella Newport and Typhimurium were the most frequently detected serovars in pond water and PL amendment samples, respectively. Interestingly, while these factors increased the likelihood of Salmonella detection in tomato plots (rhizosphere and leaves), all tomato fruits sampled (n = 4800) from these plots were Salmonella negative. Contamination of tomato fruits was extremely low (< 1%) even when tomato plots were artificially inoculated with an attenuated Salmonella Newport strain (104 CFU/mL). Furthermore, Salmonella was not detected in tomato plots irrigated using well water and amended with PL ash or TSP. Production practices also influenced the likelihood of Salmonella detection in tomato plots. Salmonella detection was higher in tomato leaf samples for NW plots, compared to SP and SW plots. This study provides evidence that attention to agricultural inputs and production practices may help reduce the likelihood of Salmonella contamination in tomato fields.

Keywords: Salmonella; agricultural practices; irrigation; poultry litter; tomato fields.

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Figures

FIGURE 1
FIGURE 1
Most probable number (MPN) values of Salmonella spp. in irrigation pond water at Virginia Tech ESAREC from August 2012 to December 2013 (A) monthly detection; in 2014 (B) weekly detection; and in 2015 (C) weekly detection. Bars present 95% confidence intervals. Brackets cover the range of growth seasons of field trials performed in the 4-year study.
FIGURE 2
FIGURE 2
Salmonella population density (MPN/kg) in poultry litter (PL) samples in different broiler farms tested in 2012 (A) and in different PL and PL ash samples in 2013 (B). Letters represent different chicken farms, and numbers behind represent different chicken houses in each farm. PL samples were collected from 14 chicken houses in 3 broiler farms in 2012 (A). In 2013, moist and dry PL was sampled from 5 chicken houses in broiler farm D. PL ash was collected from 4 factories for Salmonella detection (B). Fresh PL was collected from the circled chicken houses for soil amendment in 2012 (A) and 2013 (B) field trials of experiment 2. Bars represent 95% confidence intervals of Salmonella MPN values of tested samples.
FIGURE 3
FIGURE 3
Salmonella population density (in 2012 (A), 2013 (C), and 2014 (E) field trials) and percent contaminated (in 2012 (B), 2013 (D), and 2014 (F) field trials) plant rhizosphere samples from pond water irrigated plots under different production practices in experiment 1: staked with plastic mulch (SP), staked without plastic mulch (SW), and non-staked without plastic mulch (NW). Bars represent the 95% confidence intervals of Salmonella MPN values in plant rhizosphere.
FIGURE 4
FIGURE 4
Salmonella population density (in 2012 (A), 2014 (C), and 2015 (E) field trials) and percent contaminated (in 2012 (B), 2014 (D), and 2015 (F) field trials) plant rhizosphere samples from tomato plots fertilized with fresh PL under different production practices in experiment 2. Bars represent 95% confidence intervals.
FIGURE 5
FIGURE 5
Salmonella population density (in 2014 (A), and 2015 (C) filed trials) and percent contaminated (in 2014 (B), and 2015 (D) filed trials) plant rhizosphere samples from experimental plots irrigated by Pond/Well water and fertilized with PL or triple superphosphate (TSP, conventional fertilizer) in experiment 3. Bars represent 95% confidence intervals.
FIGURE 6
FIGURE 6
Salmonella population density (A) and percent contaminated (B) plant rhizosphere samples from tomato plots inoculated with attenuated Salmonella Newport strain SN#17 in the middle of August. The field trial of experiment 4 was performed in the growth season of 2014. Bars represent 95% confidence intervals.
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