Green Onions: Potential Mechanism for Hepatitis A Contamination

Chancellor, David D.; Tyagi, Shachi; Bazaco, Michael C.; Bacvinskas, Sara; Chancellor, Michael B.; Dato, Virginia; Miguel, Fernando de

doi:10.4315/0362-028x-69.6.1468

Cited by 54 publications

(32 citation statements)

References 10 publications

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“…Calicivirus was occasionally detected in the edible parts of romaine lettuce grown hydroponically or in soil with total virus inoculums of 10 6 to 10 9 RT-qPCR U; in similar experiments using human norovirus, no virus was found in any plants, indicating that the frequency of contamination via roots was rare even when plants were exposed to high concentrations of virus (21). However, Chancellor et al (4) showed 100% positive detection of hepatitis A virus RNA inside green onions grown in soil as well as hydroponically. Poliovirus was recovered from the leaves of tomatoes grown in soil injected with only 10 3 to 10 4 PFU/ml virus once every week (17).…”

Section: Discussionmentioning

confidence: 93%

“…Previous results are inconsistent among the studies that have been conducted assessing the impact of internalization of human enteric viruses or bacteriophage into produce during hydroponic or traditional growth conditions (4,17,21,22). It was reported that Ͻ2 log PFU of bacteriophage f2/g plant tissue was detected in the shoots of hydroponically growing bean (Phaseolus vulgaris L.) challenged with ϳ10 10 PFU/ml f2 at roots (22).…”

Section: Discussionmentioning

confidence: 99%

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Internalization of Murine Norovirus 1 by Lactuca sativa during Irrigation

Wei

Jin

Sims

et al. 2011

Appl Environ Microbiol

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Romaine lettuce (Lactuca sativa) was grown hydroponically or in soil and challenged with murine norovirus 1 (MNV) under two conditions: one mimicking a severe one-time contamination event and another mimicking a lower level of contamination occurring over time. In each condition, lettuce was challenged with MNV delivered at the roots. In the first case, contamination occurred on day one with 5 ؋ 10 8 reverse transcriptase quantitative PCR (RT-qPCR) U/ml MNV in nutrient buffer, and irrigation water was replaced with virus-free buffer every day for another 4 days. In the second case, contamination with 5 ؋ 10 5 RT-qPCR U/ml MNV (freshly prepared) occurred every day for 5 days. Virus had a tendency to adsorb to soil particles, with a small portion suspended in nutrient buffer; e.g., ϳ8 log RT-qPCR U/g MNV was detected in soil during 5 days of challenge with virus inoculums of 5 ؋ 10 8 RT-qPCR U/ml at day one, but <6 log was found in nutrient buffer on days 3 and 5. For hydroponically grown lettuce, ϳ3.4 log RT-qPCR U of viral RNA/50 mg of plant tissue was detected in some lettuce leaf samples after 5 days at high MNV inoculums, significantly higher than the internalized virus concentration (ϳ2.6 log) at low inoculums (P < 0.05). For lettuce grown in soil, approximately 2 log RT-qPCR U of viral RNA/50 mg of plant tissue was detected in lettuce with both high and low inoculums, showing no significant difference. For viral infectivity, infectious MNV was found in lettuce samples challenged with high virus inoculums grown hydroponically and in soil but not in lettuce grown with low virus inoculums. Lettuce grown hydroponically was further incubated in 99% and 70% relative humidities (RH) to evaluate plant transpiration relative to virus uptake. More lettuce samples were found positive for MNV at a significantly higher transpiration rate at 70% RH, indicating that transpiration might play an important role in virus internalization into L. sativa.

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Section: Discussionmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Internalization of Murine Norovirus 1 by Lactuca sativa during Irrigation

Wei

Jin

Sims

et al. 2011

Appl Environ Microbiol

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“…As most viral contamination would be from external sources during spraying or irrigation, a critical factor influencing the decision to analyze vegetables, whole or chopped, would be whether the claims that viruses can enter plants through root damage are substantiated or not. It appears that internal contamination of the leaves of tomato plants and green onions can occur (Oron et al 1995;Chancellor et al 2006) and that the internal contamination is of a much lower level than external contamination (Carter 2005;Urbanucci et al 2009). …”

Section: Sampling For Viruses Associated With Foodmentioning

confidence: 99%

“…Some authors have reported the presence of viral particles trapped inside vegetables taken up intracellularly through the roots (Oron et al 1995;Chancellor et al 2006;Carter 2005;Urbanucci et al 2009). This mechanism warrants further examination, and if confirmed, it will change future approaches for the detection of viruses from vegetables.…”

Section: Virus Release From Food Matricesmentioning

confidence: 99%

Analytical Methods for Virus Detection in Water and Food

et al. 2010

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Potential ways to address the issues that relate to the techniques for analyzing food and environmental samples for the presence of enteric viruses are discussed. It is not the authors' remit to produce or recommend standard or reference methods but to address specific issues in the analytical procedures. Foods of primary importance are bivalve molluscs, particularly, oysters, clams, and mussels; salad crops such as lettuce, green onions and other greens; and soft fruits such as raspberries and strawberries. All types of water, not only drinking water but also recreational water (fresh, marine, and swimming pool), river water (irrigation water), raw and treated sewage are potential vehicles for virus transmission. Well over 100 different enteric viruses could be food or water contaminants; however, with few exceptions, most well-characterized foodborne or waterborne viral outbreaks are restricted to hepatitis A virus (HAV) and calicivirus, essentially norovirus (NoV). Target viruses for analytical methods include, in addition to NoV and HAV, hepatitis E virus (HEV), enteroviruses (e.g., poliovirus), adenovirus, rotavirus, astrovirus, and any other relevant virus likely to be transmitted by food or water. A survey of the currently available methods for detection of viruses in food and environmental matrices was conducted, gathering information on protocols for extraction of viruses from various matrices and on the various specific detection techniques for each virus type.

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“…Ward and Mahler reported that the uptake and transfer of bacteriophage f2 occurred rapidly in bean plants within 16 h after exposure, and virus reached the maximal levels in stems and upwards in leaves via cut roots (20), whereas DiCaprio et al used Romaine lettuce in a hydroponic growth system with one-time-inoculated water with aeration, and they found that MNV internalized in Romaine lettuce increased and reached the peak titer on day 3 post-water inoculation (18). Chancellor et al used fluorescent microspheres to investigate hepatitis A virus uptake in green onions and determined that florescence accumulated and nearly doubled between days 1 and 2 and reached a plateau at day 7 (32). In this study, higher titers of MNV reached peaks within a shorter time in both microgreen edible tissues and roots.…”

Section: Discussionmentioning

confidence: 99%

Survival and Transfer of Murine Norovirus within a Hydroponic System during Kale and Mustard Microgreen Harvesting

Wang

Kniel

2016

Appl Environ Microbiol

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Hydroponically grown microgreens are gaining in popularity, but there is a lack of information pertaining to their microbiological safety. The potential risks associated with virus contamination of crops within a hydroponic system have not been studied to date. Here a human norovirus (huNoV) surrogate (murine norovirus [MNV]) was evaluated for its ability to become internalized from roots to edible tissues of microgreens. Subsequently, virus survival in recirculated water without adequate disinfection was assessed. Kale and mustard seeds were grown on hydroponic pads (for 7 days with harvest at days 8 to 12), edible tissues (10 g) were cut 1 cm above the pads, and corresponding pieces (4 cm by 4 cm) of pads containing only roots were collected separately. Samples were collected from a newly contaminated system (recirculated water inoculated with ϳ3 log PFU/ml MNV on day 8) and from a previously contaminated system. (A contaminated system without adequate disinfection or further inoculation was used for production of another set of microgreens.) Viral titers and RNA copies were quantified by plaque assay and real-time reverse transcription (RT)-PCR. The behaviors of MNV in kale and mustard microgreens were similar (P > 0.05). MNV was detected in edible tissues and roots after 2 h postinoculation, and the levels were generally stable during the first 12 h. Relatively low levels (ϳ2.5 to ϳ1.5 log PFU/sample of both edible tissues and roots) of infectious viruses were found with a decreasing trend over time from harvest days 8 to 12. However, the levels of viral RNA present were higher and consistently stable (ϳ4.0 to ϳ5.5 log copies/sample). Recirculated water maintained relatively high levels of infectious MNV over the period of harvest, from 3.54 to 2.73 log PFU/ml. Importantly, cross-contamination occurred easily; MNV remained infectious in previously contaminated hydroponic systems for up to 12 days (2.26 to 1.00 PFU/ml), and MNV was detected in both edible tissues and roots. Here we see that viruses can be recirculated in water, even after an initial contamination event is removed, taken up through the roots of microgreens, and transferred to edible tissues. The ease of product contamination shown here reinforces the need for proper sanitation. Hydroponics is gaining in popularity, with consistent growth across the United States (1). Specifically growing microgreens hydroponically is a new trend in the food industry (1). Microgreens have been defined as salad crop shoots harvested for consumption within 10 to 20 days of seedling emergence (2). Microgreens are considered a gourmet food to add taste, color, and texture to dishes; they mainly appear in fine and upscale restaurants and have been gaining attention and popularity during the past few years due to the fresh appearance and health benefits (3, 4). Both microgreens and sprouts are usually grown within indoor facilities under controlled environmental conditions to minimize potential contamination of foodborne pathogens. However, microgreens are different ...

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Green Onions: Potential Mechanism for Hepatitis A Contamination

Cited by 54 publications

References 10 publications

Internalization of Murine Norovirus 1 by Lactuca sativa during Irrigation

Internalization of Murine Norovirus 1 by Lactuca sativa during Irrigation

Analytical Methods for Virus Detection in Water and Food

Survival and Transfer of Murine Norovirus within a Hydroponic System during Kale and Mustard Microgreen Harvesting

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