Assessment of region, farming system, irrigation source and sampling time as food safety risk factors for tomatoes

Pagadala, S; Marine, Sasha C.; Micallef, Shirley A.; Wang, Fei; Pahl, Donna M.; Melendez, Meredith; Kline, Wesley L.; Oni, Ruth A.; Walsh, Christopher S.; Everts, Kathryne L.; Buchanan, Robert L.

doi:10.1016/j.ijfoodmicro.2014.12.005

Cited by 86 publications

(73 citation statements)

References 30 publications

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“…In our study, only one pond sediment sample was culture confirmed for Salmonella. This low pathogen prevalence in the environment agrees with our previous survey on mid-Atlantic tomato farms performed in summer of 2012, where no Salmonella or STEC was isolated from 163 environmental samples from the same region (36).…”

Section: Discussionsupporting

confidence: 91%

“…Previous surveys report no difference in pathogen prevalence due to production scale (25) or between conventionally and organically grown produce (34,35), although in the latter study, two "semiorganic" samples were contaminated with Salmonella (34). Our own work with tomatoes cultivated in the mid-Atlantic region found that farming system was not a significant factor for indicator bacteria or enteric pathogens (36).…”

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confidence: 48%

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The Growing Season, but Not the Farming System, Is a Food Safety Risk Determinant for Leafy Greens in the Mid-Atlantic Region of the United States

Marine

Pagadala

Wang

et al. 2015

Appl Environ Microbiol

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Small-and medium-size farms in the mid-Atlantic region of the United States use varied agricultural practices to produce leafy greens during spring and fall, but the impact of preharvest practices on food safety risk remains unclear. To assess farm-level risk factors, bacterial indicators, Salmonella enterica, and Shiga toxin-producing Escherichia coli (STEC) from 32 organic and conventional farms were analyzed. A total of 577 leafy greens, irrigation water, compost, field soil, and pond sediment samples were collected. Salmonella was recovered from 2.2% of leafy greens (n ‫؍‬ 369) and 7.7% of sediment (n ‫؍‬ 13) samples. There was an association between Salmonella recovery and growing season (fall versus spring) (P ‫؍‬ 0.006) but not farming system (organic or conventional) (P ‫؍‬ 0.920) or region (P ‫؍‬ 0.991). No STEC was isolated. In all, 10% of samples were positive for E. coli: 6% of leafy greens, 18% of irrigation water, 10% of soil, 38% of sediment, and 27% of compost samples. Farming system was not a significant factor for levels of E. coli or aerobic mesophiles on leafy greens but was a significant factor for total coliforms (TC) (P < 0.001), with higher counts from organic farm samples. Growing season was a factor for aerobic mesophiles on leafy greens (P ‫؍‬ 0.004), with higher levels in fall than in spring. Water source was a factor for all indicator bacteria (P < 0.001), and end-of-line groundwater had marginally higher TC counts than source samples (P ‫؍‬ 0.059). Overall, the data suggest that seasonal events, weather conditions, and proximity of compost piles might be important factors contributing to microbial contamination on farms growing leafy greens. Increased awareness of the nutritional and economic benefits of eating fresh produce has caused global consumption to increase 4.5% from 1990 to 2004 (1), but field-grown foods such as vegetables and leafy greens (including lettuce, spinach, spring mix, and kale) can also serve as reservoirs of microorganisms, including bacteria, molds, and yeasts. Most of these microorganisms are not harmful and are part of the background microflora of the plant. However, human-pathogenic bacteria such as Salmonella, Listeria monocytogenes, Shigella spp., and Escherichia coli O157:H7 have been associated with foodborne outbreaks involving fresh produce (2). The ability of foodborne pathogens to colonize and persist as part of the plant microbiome as endophytes or epiphytes (reviewed in reference 3) represents a significant food safety risk, as fresh produce is often consumed raw without any processing "kill step."In the United States, estimates calculate approximately 4.9 million yearly incidents of food-related illnesses attributed to plant commodities, with leafy vegetables comprising 22.3% of these (4). Following the E. coli O157:H7 multistate outbreak in fall 2006, which was attributed to spinach (5), leafy greens have received significant attention from government, industry, and academic researchers. Other incidents have implicated leafy greens as a vehicl...

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Section: Discussionsupporting

confidence: 91%

contrasting

confidence: 48%

The Growing Season, but Not the Farming System, Is a Food Safety Risk Determinant for Leafy Greens in the Mid-Atlantic Region of the United States

Marine

Pagadala

Wang

et al. 2015

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

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“…The reason for these inconsistent sporadic relationships was unclear but is likely associated with the use of groundwater and perforated hoses for irrigation, both of which reduce contamination risk (43,44). Although microbial indicators were found in water, levels were below U.S. Food and Drug Administration (FDA) Food Safety Modernization Act (FSMA) Final Rule on Produce Safety standard limits (28,31,45); this is consistent with other studies demonstrating that groundwater carries a relatively low risk of pathogen detection, compared to that of surface water (9,46). Regardless, our results do not support a positive relationship between indicator detection or concentration on produce and that in source (i.e., groundwater) and irrigation (drip) water.…”

Section: Discussionsupporting

confidence: 81%

“…Outbreak investigations on the farm and in packing facilities suggest that sources of produce contamination may include animal droppings, farmworkers' hands (subsequently simply referred to as "hands"), soil, agricultural water, tools, equipment, and other contact surfaces (6)(7)(8)(9)(10)(11)(12). Under laboratory conditions, such contamination events have been demonstrated (13)(14)(15)(16).…”

mentioning

confidence: 99%

Contamination of Fresh Produce by Microbial Indicators on Farms and in Packing Facilities: Elucidation of Environmental Routes

Bartz

Lickness

Heredia

et al. 2017

Appl Environ Microbiol

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To improve food safety on farms, it is critical to quantify the impact of environmental microbial contamination sources on fresh produce. However, studies are hampered by difficulties achieving study designs with powered sample sizes to elucidate relationships between environmental and produce contamination. Our goal was to quantify, in the agricultural production environment, the relationship between microbial contamination on hands, soil, and water and contamination on fresh produce. In 11 farms and packing facilities in northern Mexico, we applied a matched study design: composite samples (n ϭ 636, equivalent to 11,046 units) of produce rinses were matched to water, soil, and worker hand rinses during two growing seasons. Microbial indicators (coliforms, Escherichia coli, Enterococcus spp., and somatic coliphage) were quantified from composite samples. Statistical measures of association and correlations were calculated through Spearman's correlation, linear regression, and logistic regression models. The concentrations of all microbial indicators were positively correlated between produce and hands ( range, 0.41 to 0.75; P Ͻ 0.01). When E. coli was present on hands, the handled produce was nine times more likely to contain E. coli (P Ͻ 0.05). Similarly, when coliphage was present on hands, the handled produce was eight times more likely to contain coliphage (P Ͻ 0.05). There were relatively low concentrations of indicators in soil and water samples, and a few sporadic significant associations were observed between contamination of soil and water and contamination of produce. This methodology provides a foundation for future field studies, and results highlight the need for interventions surrounding farmworker hygiene and sanitation to reduce microbial contamination of farmworkers' hands.IMPORTANCE This study of the relationships between microbes on produce and in the farm environment can be used to support the design of targeted interventions to prevent or reduce microbial contamination of fresh produce with associated reductions in foodborne illness.

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“…Moreover, organic fertilization is often alleged to be a high-risk practice. Pagadala et al (2015) [7] reported that manure amendment enhanced the possibility of the presence of Salmonella in the field up to a year following application. Use of dairy manure was also found to increase the risk of spinach contamination with generic Escherichia coli.…”

Section: Introductionmentioning

confidence: 99%

Organic Cultivation of Tomato in India with Recycled Slaughterhouse Wastes: Evaluation of Fertilizer and Fruit Safety

et al. 2015

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Environmental and health safety of recycled slaughterhouse wastes-derived fertilizer and the produce obtained through its application is not well understood. Waste bovine blood and rumen digesta were mixed, cooked and sun-dried to obtain bovine-blood-and-rumen-digesta-mixture (BBRDM, NPK 30.36:1:5.75). 1.26 ± 0.18 log CFU mL −1 fecal coliforms were recovered in BBRDM. E. coli O157:H7, Mycobacteria, Clostridium sp., Salmonella sp., Bacillus sp. and Brucella sp. were absent. No re-growth of pathogens was observed after 60 days storage in sealed bags and in the open. However, prions and viruses were not evaluated. Heavy metals (Pb, Cr, Cd, Cu, Zn, As, Ni, Mn) concentrations in BBRDM were within internationally permissible limits. BBRDM was applied for field cultivation of tomato during 2012-2013 and 2013-2014. Lycopene and nitrate contents of BBRDM-grown tomatoes were higher than Diammonium OPEN ACCESSAgriculture 2015, 5 827 phosphate (DAP) + potash-grown tomatoes because BBRDM supplied 2.5 times more the amount of nitrogen than DAP (NPK 18:46:0) + potash (NPK 0:0:44). Heavy metals and nitrate/nitrite concentrations in tomatoes were within internationally acceptable limits. BBRDM-grown tomatoes showed no mutagenic activity in the Ames test. Sub-acute toxicity tests on Wistar rats fed with BBRDM-grown tomatoes did not show adverse clinical picture. Thus, no immediate environmental or health risks associated with BBRDM and the tomatoes produced were identified.

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Assessment of region, farming system, irrigation source and sampling time as food safety risk factors for tomatoes

Cited by 86 publications

References 30 publications

The Growing Season, but Not the Farming System, Is a Food Safety Risk Determinant for Leafy Greens in the Mid-Atlantic Region of the United States

The Growing Season, but Not the Farming System, Is a Food Safety Risk Determinant for Leafy Greens in the Mid-Atlantic Region of the United States

Contamination of Fresh Produce by Microbial Indicators on Farms and in Packing Facilities: Elucidation of Environmental Routes

Organic Cultivation of Tomato in India with Recycled Slaughterhouse Wastes: Evaluation of Fertilizer and Fruit Safety

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