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

Abstract

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...

Microbiology of organic and conventionally grown fresh produce

“…Only Ceuppens et al, 51 Marine et al, 54 Mukherjee et al 55 and Tango et al 59 detected pathogenic bacteria in the fresh produce samples analyzed above. Ceuppens et al 51 isolated Salmonella from one organic lettuce sample.…”

“…Studies have isolated pathogens including Salmonella spp., L. monocytogenes and pathogenic E. coli from fresh and fresh-cut vegetable samples in many countries 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49. Other studies have compared the microbiological quality of vegetables from organic and conventional production 21, 22, 24, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59. Ceuppens et al 51 assessed the microbiological quality of lettuce production in Brazil and detected generic E. coli more frequently and at higher average concentrations in lettuce samples from organic farms (23.1% and 3.22 log CFU/g) vs. conventional farms (16.7% and 2.27 log CFU/g).…”

“…Khalil and Gomaa 53 analyzed 380 samples of unpackaged whole conventional and 84 packaged whole organic leafy greens collected from retail markets in Alexandria, Egypt, and observed the mean total bacterial count for organic samples were statistically significantly less ( p  < 0.05) than those of the corresponding conventional samples and E. coli was detected in 100% of all leafy greens. Marine et al 54 evaluated leafy greens from organic ( n  = 178) and conventional ( n  = 191) farms in the Mid-Atlantic Region of the United States. They observed that the farming system was not a significant factor for E. coli , aerobic mesophiles or Salmonella , but with (non-statistically significant) higher total coliform counts from organic farm samples.…”

Microbiological safety of organic and conventional foods

“…Use of organic fertilizers according to good agricultural practice (GAP) does not increase the rate of contamination of fresh produce by enteric pathogens (Alsanius, 2014) or Escherichia coli (literature data summarized by Smith-Spangler et al, 2012). As learned from outbreaks and field studies, the main risk factors are use of irrigation water that had been contaminated by human or livestock excreta (Park et al, 2012), and handling of produce by carriers of pathogens, but not the farming system (Marine et al, 2015). Some outbreaks have been reported in which leafy vegetables were shown or suspected to be involved (CDC, 2016).…”

“…heavy rainfall and flooding) and handling of food by human carriers of pathogens. To quote from Marine et al (2015), the farming system is not a food safety risk determinant for leafy greens.…”