2. Controlled Environment Agriculture (CEA) and Food Safety
3. Pathogen Internalization in Leafy Vegetables
4. Hydroponic System Designs
5. Pathogen Internalization in Hydroponic Systems
5.1. Deep Water Culture
5.2. Nutrient Film Technique
5.3. Other Hydroponic Systems
6. Targeted Preventive Controls in Hydroponic Systems for Leafy Vegetables
6.1. Production Water Quality and Whole System Decontamination
6.1.1. Current Agricultural Water Quality Guidelines for Fresh Produce
6.1.2. Risk of System Contamination
6.1.3. Water Treatment Strategies
6.2. Minimizing Root Damage
6.3. Biological Control
6.4. Plant Cultivar Selection
7. Potential Actual Health Risk from Consumption of Leafy Vegetables with Internalized Pathogens
- Development of standard guidelines for lab-scale hydroponic cultivation of leafy vegetables to enable study comparison. This includes seed germination protocols, best practices for water management, and design specifications for each type of hydroponic system.
- Determine appropriate pathogen inoculation concentrations and methods for the research question being addressed. Should there be a range of concentrations considered? How does the inoculation of the seed at germination versus inoculation of the nutrient solution change the interpretation of the results?
- Does the presence of a solid substrate impact colonization efficiency? Is there a differential effect between contamination of the substrate and the contamination of nutrient water flowing through it?
- Standardization of microbial extraction methods from plants to ensure the recovery of truly endophytic microorganisms.
- Selection of microorganisms should be standardized. For instance, surrogate microorganisms should be validated as representative of their human pathogen counterparts. Strains of human pathogens should also be carefully considered and validated for use in hydroponic cultivation systems.
- Given the variation in the susceptibility of plants to pathogen colonization, the selection of plant cultivars should be standardized to represent commercially relevant cultivars, and the validation of cultivars used in hydroponic research is needed.
Conflicts of Interest
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|Nutrient Film Technique||Continuous Drip||Wick Method||Flood and Drain||Conventional, Field-based|
|Submergence of plant roots in nutrient solution|
|Roots are fully submerged in NS throughout the growing process.||Root tips touch a 1–10-mm film of NS running along the bottom of plastic gutters.||Roots grow through a solid matrix in a grow bed that is filled with NS.||Roots are fully submerged in NS throughout the growing process.||Roots grow through a solid matrix in a grow bed that is mostly filled with NS when flooded, and exposed to air when not flooded.||Roots are fully covered by the soil matrix and exposed to water through irrigation.|
|No water flow||NS is actively pumped continuously or intermittently at a low flow rate.||NS is actively pumped continuously at a low flow rate.||No water flow in plant reservoir. NS is passively replenished through capillary action from the tank up through fibrous wicks.||Grow bed is periodically flooded with NS at a higher flow rate than NFT or drip, by active pumping, and then drained. The pump is typically timer-controlled.||Roots grow in soil and are watered by drip irrigation and surface watering.|
|No||No||Yes||Yes||Yes||Soil, compost, manure|
|Method of root aeration|
|Injection||All but the root tips are exposed to the air inside the gutters.||Agitation from pump||Injection||Exposed to air during drained periods, from agitation by the pump during flood periods.||By ensuring adequate soil drainage|
|System Type||Solid Phase||Pathogen||Plant||Inoculation||Surface Sterilized||Compared with Soil||Internalization Outcome||Ref.|
|HA-GB||N/A||E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes||Carrot, cress, lettuce, radish, spinach and tomato||Seeds soaked in 2 log CFU/mL, and then air-dried on sterile filter paper for 2 h at ~22 °C||Yes||No||Levels of all pathogens increased from 2 log to ~5–6 log CFU during 10-day germination. Counts and SEM showed a plant-specific effect (cress and radish most susceptible), a pathogen-specific effect (L. monocytogenes most abundant), and an age-specific effect (internalization was greater in young plants)|||
|DWC-L-T||No||E. coli TG1 expressing GFP||Corn seedlings (Zea mays)||7 log CFU/mL added directly to the 4-L tray of nutrient solution||No||No||Internalized E. coli TG1 detected in shoots. Entire root system removed (430 CFU/g), root tips severed (500 CFU/g), undamaged plants (18 CFU/g).|||
|DWC-L-F||No||GFP-expressing E. coli O157:H7 and S. Typhimurium (MAE 110 and 119)||Lettuce (Lactuca sativa cv. Tamburo)||29 mL of hydroponic nutrient solution with a final concentration of 7 log CFU/mL||Yes||Yes||Hydroponic: S. Typhimurium MAE 119 internalized at 5 log CFU/g.|||
|DWC-L-T||No||GFP-expressing E. coli O157:H7 from a spinach outbreak and a beef outbreak as well as a non-pathogenic clinical E. coli isolate||Spinach||3 and 7 log CFU/mL or g added directly to the nutrient solution or soil. Group 1: Inoculated hydroponic for 21 d; Group 2: Hydroponic for 21 d, transplanted into sterile soil; Group 3: hydroponic for 21 d, transplanted into inoculated soil||Yes||Yes||At both 4 log and 7 log CFU/mL in hydroponic water, between 2–4 log CFU/shoot internalized pathogen detected at cultivation day 14. Soil recovery was negligible for both high and low inocula and required enrichment to detect. 23/108 soil-grown plants showed E. coli in root tissues, but no internalization in shoots.|||
|DWC-L-F||Sand||S. Typhimurium (LT1 and S1) and L. monocytogenes sv4b, L. ivanovii, L. innocua||Barley (Hordeum vulgare)||8 log CFU/mL suspension per bacterial species added directly to the surface of the sand 1 to 2 days after planting||Yes||No||Salmonella internalized in roots, stems, and leaves, while Listeria spp. only colonized the root hairs.|||
|DWC-L-C||No||Six strains of E. coli O157:H7, five strains of S. Typhimurium and S. Enteritidis, six strains of L. monocytogenes||Spinach (Brassica rapa var. perviridis)||3 or 6 log CFU/mL added directly to the hydroponic water solution||No||No||Across all microorganisms, the 3 log CFU/mL had an average recovery of <1.7 log CFU/leaf in 7/72 samples. The 6 log CFU/mL inoculum resulted in better recovery (50/76 samples) in a range of 1.7 to 4.4 log CFU/leaf.|||
|DWC-L-T||No||E. coli O157:H7||Spinach cultivars Space and Waitiki||5 or 7 log CFU/mL added directly to the Hoagland medium. Hoagland medium was re-inoculated as needed to maintain initial bacterial levels.||Yes||Yes||E. coli O157:H7 internalized in 15/54 samples at 7 days after inoculation with 7 log CFU/mL. Neither curli or spinach cultivar had an impact on the internalization rate.|||
|DWC-L-J||Vermiculite||Coxsackievirus B2||Lettuce (L. sativa)||7.62–9.62 log genomic copies/L in water solution||Unknown||No||Virus detected in leaves on the first day at all inoculation levels; however, decreased to below LOD over the next 3 days.|||
|NFT||Rockwool plugs||E. coli P36 (fluorescence labeled)||Spinach (Spinacia oleracea L. cv. Sharan)||2 to 3 log CFU/mL E. coli added to the nutrient solution in the holding tank. 2 log CFU/g was added to soil.||Yes||Yes||For hydroponic: total surface (7.17 ± 1.39 log CFU/g), internal (4.03 ± 0.95 log CFU/g). For soil: total surface (6.30± 0.64 log CFU/g), internal (2.91± 0.81 log CFU/g)|||
|NFT||No||MNV||Kale microgreens (Brassica napus) and mustard microgreens (Brassica juncea)||Nutrient solution containing ~3.5 log PFU/mL on day 8 of growth||Unknown||No||MNV was internalized into roots and edible tissues of both microgreens within 2 h of nutrient solution inoculation in all samples at 1.98 to 3.47 log PFU/sample. After 12 days, MNV remained internalized and detectable in 27/36 samples at 1.42 to 1.61 log PFU/sample.|||
|DS||Peat pellets/clay pebbles||MNV (type 1), S. Thompson (FMFP 899)||Basil (Ocimum basilicum)||MNV (8.46 log-PFU/mL) or S. Thompson (8.60 log-CFU/mL) via soaking the germinating discs for 1 h||No||No||MNV was internalized into edible parts of basil via the roots with 400 to 580 PFU/g detected at day 1 p.i., and the LOD was reached by day 6. Samples were positive for S. Thompson on days 3 and 6 post-enrichment.|||
|DWC||No||Citrobacter freundii PSS60, Enterobacter spp. PSS11, E. coli PSS2, Klebsiella oxytoca PSS82, Serratia grimesii PSS72, Pseudomonas putida PSS21, Stenotrophomonas maltophilia PSS52, L. monocytogenes ATCC 19114||Radish (R. sativus L.) microgreens||Final concentration of 7 log CFU/mL for each bacterium added directly to the nutrient solution||Yes||No||C. freundii PSS60, Enterobacter spp. PSS11, K. oxytoca PSS82 were suspected to have internalized in hypocotyls. These three strains were detected with and without the surface sterilization of plant samples.|||
|HA-TT||N/A||Klebsiella pneumoniae 342, Salmonella Cubana, Infantis, 8137, and Typhimurium; E. coli K-12, E. coli O157:H7||Alfalfa (M. sativa) and Barrelclover (M. truncatula)||1 to 7 log CFU/mL added directly to the growth medium at the seedling root area after 1 day of germination.||Yes||No||K. pneumoniae 342 colonized root tissue at low inoculation levels. S. Cubana H7976 colonized at high inoculation levels. No difference between Salmonella serovars|||
|HA-TT||N/A||S. Dublin, Typhimurium, Enteritidis, Newport, Montevideo||Lettuce (Lactuca sativa cv. Tamburo, Nelly, Cancan)||10 µL of a 7 log CFU/mL suspension per serovar added directly to the 0.5% Hoagland’s water agar containing two-week old seedlings||Yes||Yes||Hydroponic: S. Dublin, Typhimurium, Enteritidis, Newport, and Montevideo internalized in L. sativa Tamburo at 4.6 CFU/g, 4.27 CFU/g, 3.93 CFU/g, ~3 CFU/g, and ~4 log CFU/g, respectively|||
|DWC||No||hNoV GII.4 isolate 5 M, MNV, and TV||Romaine lettuce (Lactuca sativa)||TV and MNV (6 log PFU/mL), and hNoV (6.46 log RNA copies/mL) added directly to the nutrient solution||Yes||No||TV, MNV, and hNoV detected in leaves within 1 day. At day 14, recovery levels were TV: 5.8 log PFU/g, MNV: 5.5 log PFU/g, and hNoV: 4 log RNA copies/g were recovered|||
|DWC||Vermiculite||E. coli O157:H7||Red sails lettuce (Lactuca sativa)||Started with 7 log CFU/mL and maintained in water at 5 log CFU/mL||Yes||No||E. coli O157:H7 internalized in contaminated lettuce of cut and uncut roots. Mean uncut: 2.4 ± 0.7; Mean 2 cuts: 4.0 ± 1.9; Mean 3 cuts: 3.3 ± 1.3. No significant difference was found between two and three cuts.|||
|DWC-(AP)||Vermiculite||Total coliforms||Red sails lettuce (Lactuca sativa)||No inoculation. Detected 2 to 4 log CFU/mL natural concentration of coliform bacteria in a pilot system downstream of a cattle pasture||Yes||No||UV light at 96.6% transmittance and a flow rate of 48.3 L/min reduced total coliforms by 3 log CFU/mL in water. Internalized coliform was not recovered from either samples or control lettuce.|||
|Membrane filtration||Precise filtration, can choose pore size to suit needs||Reduced flow rate, easy clogging|
|Slow sand filtration||Most common, inexpensive, a variety of substrate choices.||May not effectively remove pathogens on its own|
|UV light treatment||Can be combined with slow sand filtration for high efficiency||Water needs high clarity, so must be combined with sediment filter to ensure maximum light penetration|
|Chlorination||Inexpensive, standard recommendation||Storage issues, toxic to humans|
|Iodine||Less toxic than chlorine||Need high doses to be effective, costly|
|Hydrogen peroxide||Less toxic than chlorine, weak oxidizer||Need high doses to be effective, costly|
|Ozonation||Non-toxic to humans, no residues left behind||Strong oxidizer may cause hydroponic mineral nutrients to precipitate, reducing bioavailability|
|Biological control agents||Takes advantage of natural features of the system to suppress pathogens without addition of harsh chemicals||Inconsistent, difficult to maintain microbial numbers to sufficiently suppress pathogens, manipulation of microbiome for this purpose still a poorly understood research area.|
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