Abiotic Stress and Phyllosphere Bacteria Influence the Survival of Human Norovirus and Its Surrogates on Preharvest Leafy Greens

Esseili, Malak A.; Gao, Xiang; Tegtmeier, Sarah; Saif, Linda J.; Wang, Qiuhong

doi:10.1128/aem.02763-15

Cited by 18 publications

(17 citation statements)

References 73 publications

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“…Such interactions have important consequences for both plant and food animal diseases, but also for food borne human pathogens. The ability for a pathogenic virus to form a complex with the normal flora of the plant or human and animal commensals introduced in irrigation water could allow the stabilization of that virus through food processing and shipping. Modulation of the bacterial communities on plants both in the field and during processing could represent a novel way to control foodborne illness transmission.…”

Section: Impact Of Co‐infections On Pathogen Transmissionmentioning

confidence: 99%

Close Encounters of the Viral Kind: Cross‐Kingdom Synergies at the Host–Pathogen Interface

Rowe

Rosch

2019

BioEssays

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The synergies between viral and bacterial infections are well established. Most studies have been focused on the indirect mechanisms underlying this phenomenon, including immune modulation and alterations to the mucosal structures that promote pathogen outgrowth. A growing body of evidence implicates direct binding of virus to bacterial surfaces being an additional mechanism of synergy at the host-pathogen interface. These cross-kingdom interactions enhance bacterial and viral adhesion and can alter tissue tropism. These bacterial-viral complexes play unique roles in pathogenesis and can alter virulence potential. The bacterial-viral complexes may also play important roles in pathogen transmission. Additionally, the complexes are recognized by the host immune system in a distinct manner, thus presenting novel routes for vaccine development. These synergies are active for multiple species in both the respiratory and gastrointestinal tract, indicating that direct interactions between bacteria and virus to modulate host interactions are used by a diverse array of species.

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Section: Impact Of Co‐infections On Pathogen Transmissionmentioning

confidence: 99%

Close Encounters of the Viral Kind: Cross‐Kingdom Synergies at the Host–Pathogen Interface

Rowe

Rosch

2019

BioEssays

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“…Human norovirus-like particles associate with the surface of Romaine lettuce aggregating in and around the stomata, while in green onions between the cells of the epidermis and cell walls of both the shoots and roots, what suggests that viruses differ in their localization patterns to varieties of fresh produce [15]. Also, there is a need to understand the factors influencing the survival/persistence characteristics of human norovirus on pre-harvest leafy greens to develop proper measures to prevent contamination [16]. For lettuce, as one of the most often implicated fresh vegetable in human norovirus foodborne outbreaks, many theories exist.…”

Section: Transmission and Associated Foodsmentioning

confidence: 99%

Noroviruses in food chain production

Radin¹

2016

Hrana i ishrana

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Viruses, predominantly noroviruses, are progressively identified as the leading cause of foodborne diseases worldwide. In the Europe Union they have been determined as a main cause of foodborne outbreaks in 2014, while in the United States viruses are responsible for 58% (5.5 million) of foodborne illnesses annually. Noroviruses, the etiological agent of foodborne gastroenteritis belong to the Caliciviridae family, genus Norovirus which is genetically classified into 6 established geno-groups (GI to GVI). Human noroviruses are icosahedral nonenveloped RNA viruses, approximately 27 to 38 nm in diameter, and contain single-stranded positive-sense RNA genomes size from 7.4 to 8.3 kb and 3 open reading frames. Viruses are transmitted by contaminated food or water, through person-to-person contact, and by cross-contamination from surfaces. Foods at risk includes those which need extensive handling, mostly ready-to-eat foods that do not undergo further processing, and those exposed to environmental contamination, such as seafood and fresh produce. Contamination with human norovirus can happen throughout the entire food production chain: (i) at the primary production (due to fecal polluted water in the harvest area/ irrigation/ water used to dilute pesticide, organic-based fertilizers and potential root uptake of pathogens following internalization); (ii) during harvest (contact with human feces or fecal soiled materials, cross-contamination with equipment and food handlers poor hygiene practice); (iii) at the postharvest stage by inappropriate practices during handling, processing, preparation, storage, distribution (by infected food handlers, spraying with contaminated water, cross-contamination during washing process) and (iv) at the point of sale/consumption (by infected food handlers, cross-contamination with polluted working instruments or surfaces previously contaminated by infected food handlers or food items). Strategies to reduce human noroviruses in the food chain should, beside good hygiene practice, engage interventions to prevent their adsorption to food/contact surfaces and inactivation on/within the products using successful processing techniques.

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“…In one study, HuNoV remained infectious for Ͼ60 days in water, as assessed by challenging human volunteers, while other studies reported the detection of HuNoV RNA for Ͼ2 years in water (reviewed in reference 20). HuNoV contaminating leafy green surfaces has been found to be stable for at least 2 weeks (21). This is a critical duration of time because mature leafy greens are marketable within 2 weeks.…”

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confidence: 99%

“…This is a critical duration of time because mature leafy greens are marketable within 2 weeks. Multiple factors have been found to enhance the virus survival on the leaf surface, including the presence of phytopathogens, physical damage, and/or the natural phyllosphere bacteria (21)(22)(23). Furthermore, although multiple studies investigated the possibility of HuNoV internalization to the edible leaves through the roots, the studies either were based solely on the use of surrogate viruses or reported conflicting results under similar settings or for the same produce.…”

mentioning

confidence: 99%

“…One research team has used HuNoV in their studies and found significant internalization of the virus in lettuce and green onion under hydroponic growth conditions (24,25), while another team failed to detect any internalization of HuNoV in lettuce under hydroponic or soil growth conditions (26). This discrepancy, in addition to the fact that different surrogate viruses have been found to exhibit various degrees of similarity to HuNoV on leafy greens (21,27), necessitates a better assessment of the internalization dynamics of HuNoV in leafy greens, especially lettuce. Therefore, the objectives of this study were to (i) investigate whether lettuce and spinach can internalize HuNoV into the edible leaves, (ii) simultaneously assess the behavior of surrogate viruses TV and SaV in comparison with that of HuNoV, and (iii) determine whether HuNoV particles can be visualized inside lettuce and spinach tissues.…”

mentioning

confidence: 99%

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Tissue Distribution and Visualization of Internalized Human Norovirus in Leafy Greens

Esseili

Meulia

Saif

et al. 2018

Appl Environ Microbiol

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Lettuce has been implicated in human norovirus (HuNoV) outbreaks. The virus is stable on the leaf surface for at least 2 weeks; however, the dynamics of virus internalization have not been fully investigated. The purpose of this study was to assess the internalization and distribution of HuNoV and two surrogate viruses, porcine sapovirus (SaV) and Tulane virus (TV), in lettuce and spinach. Viral inoculations through the roots of seedlings and the petiole of leaves from mature plants were performed, and the viruses were tracked on days 1 and 6 post-root inoculation and at 16 h and 72 h post-petiole inoculation. Confocal microscopy was used to visualize root-internalized HuNoV. In both lettuce and spinach, (i) HuNoV was internalized into the roots and leaves at similar RNA titers, whereas surrogate viruses were more restricted to the roots, (ii) all three viruses were stable inside the roots and leaves for at least 6 days, and (iii) HuNoV disseminated similarly inside the central veins and leaf lamina, whereas surrogate viruses were more restricted to the central veins. Infectious TV, but not SaV, was detectable in all tissues, suggesting that TV has greater stability than SaV. HuNoV was visualized inside the roots' vascular bundle and the leaf mesophyll of both plants. In conclusion, using surrogate viruses may underestimate the level of HuNoV internalization into edible leaves. The internalization of HuNoV through roots and cut leaves and the dissemination into various spinach and lettuce tissues raise concerns of internal contamination through irrigation and/or wash water. IMPORTANCE Human noroviruses are the leading cause of foodborne outbreaks, with lettuce being implicated in the majority of outbreaks. The virus causes acute gastroenteritis in all age groups, with more severe symptoms in children, the elderly, and immunocompromised patients, contributing to over 200,000 deaths worldwide annually. The majority of deaths due to HuNoV occur in the developing world, where limited sanitation exists along with poor wastewater treatment facilities, resulting in the contamination of water resources that are often used for irrigation. Our study confirms the ability of lettuce and spinach to internalize HuNoV from contaminated water through the roots into the edible leaves. Since these leafy greens are consumed with minimal processing that targets only surface pathogens, the internalized HuNoV presents an added risk to consumers. Thus, preventive measures should be in place to limit the contamination of irrigation water. In addition, better processing technologies are needed to inactivate internalized viral pathogens.

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Abiotic Stress and Phyllosphere Bacteria Influence the Survival of Human Norovirus and Its Surrogates on Preharvest Leafy Greens

Cited by 18 publications

References 73 publications

Close Encounters of the Viral Kind: Cross‐Kingdom Synergies at the Host–Pathogen Interface

Close Encounters of the Viral Kind: Cross‐Kingdom Synergies at the Host–Pathogen Interface

Noroviruses in food chain production

Tissue Distribution and Visualization of Internalized Human Norovirus in Leafy Greens

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