Internalization and dissemination of human norovirus and Tulane virus in fresh produce is plant dependent

Yang, Zhihong; Chambers, Heather; DiCaprio, Erin; Gao, Gary; Lǐ, Jiànróng

doi:10.1016/j.fm.2017.07.015

Cited by 20 publications

(15 citation statements)

References 51 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Norovirus is the leading cause of food borne illness accounting for 45% of illnesses in produce (Gould et al, 2013). Numerous studies have established that human norovirus is able to attach and internalize in a variety of row vegetable crops (Hirneisen and Kniel, 2013;DiCaprio et al, 2015a,b;Markland et al, 2017;Yang et al, 2018). These studies suggest the multiple routes in which NoV can internalize and transport to various tissues of the plant and the potential immune response of plants to these pathogens.…”

Section: Food Safety In the Twenty First Century: The Need For A New mentioning

confidence: 99%

One Health for Food Safety, Food Security, and Sustainable Food Production

Garcia

Osburn

Jay-Russell

2020

Front. Sustain. Food Syst.

184

View full text Add to dashboard Cite

Globally, our society faces an enormous challenge to feed, house, and provide a healthy life for the growing human population while preserving the environment and natural resources for the benefit of future generations. In order to meet these challenges, sustainable food production and environmental stewardship is paramount and will require a One Health approach. One Health is the concept that the health of humans, animals, and the environment are inextricably linked. This approach can be applied to food safety, sustainable food production, and environmental stewardship by bringing together interdisciplinary teams to create a One Health network to address these challenges. In order to achieve food security for the global population, preserve natural resources, and improve health through safeguarding food safety, there is a need for increased awareness among academics, producers, consumers, and government agencies in the following topics: (1) One Health Initiatives for Sustainable Food Systems, Food Safety and Food Security, (2) Brief History of Food Safety in the United States, (3) Food Safety in the Twenty First Century: The Need for a New Perspective, (4) Food Security in the Twenty First Century: Disasters and Transboundary Disease. These topics cover the need for incorporating One Health education into curriculum for scientific, engineering, and humanities programs to build capacity in One Health competencies with the goal of established networks that will work toward improving public health, food safety, and sustainable agriculture by establishing new perspectives on interactions among plants, animals, and humans and recognizing the threat of disasters and transboundary diseases to food security.

show abstract

Section: Food Safety In the Twenty First Century: The Need For A New mentioning

confidence: 99%

One Health for Food Safety, Food Security, and Sustainable Food Production

Garcia

Osburn

Jay-Russell

2020

Front. Sustain. Food Syst.

184

View full text Add to dashboard Cite

show abstract

“…Metagenomic analysis of romaine and iceberg lettuce has shown the presence of wide range of plant and animal/ human viruses already on the field [63•]. It has also been shown that NoV can be internalised by some plants such as lettuce and strawberries through the root system and can therefore be present inside the plant and fruits rather than just contaminating the surface [64,65]; similar to the internalisation and retention of acid resistant viruses in water filtering molluscs [66]. Even though being internalised, NoV, such as most animal and human viruses, is not able to infect or replicate in plant cells [67].…”

Section: Other Food-contaminating Virusesmentioning

confidence: 99%

Selected Viruses Detected on and in our Food

Bachofen

2018

Curr Clin Micro Rpt

View full text Add to dashboard Cite

Purpose of Review The purpose of this review is to provide an update on recent literature and findings concerning selected foodborne viruses. Two groups of viruses were selected: (a) the most important viruses contaminating food, based on numbers of publications in the last 5 years and (b) viruses infecting sources of food that might have an impact on human health. Recent Findings Important foodborne viruses such as norovirus, hepatitis A and rotavirus are usually "only" contaminating food and are detected on the surface of foodstuffs. However, they are threats to human public health and make up for the majority of cases. In contrast, the meaning of viruses born from within the food such as natural animal and plant viruses is still in many cases unknown. An exception is Hepatitis E virus that is endemic in pigs, transmitted via pork meat and is recognised as an emerging zoonosis in industrialised countries. Summary Even though the clinical meaning of "new" foodborne viruses, often detected by next generation sequencing, still needs clarification, the method has great potential to enhance surveillance and detection particularly in view of an increasingly globalised food trade.

show abstract

“…In the same study, the surrogate virus canine calicivirus (CaCV) did not mimic HuNoV behavior and was shown to be internalized infrequently through the roots into the leaves of lettuce seedlings (26). In contrast, another laboratory reported the internalization of HuNoV through the roots into the leaves of lettuce seedlings (3 weeks of age) and in 2-month-old green onions (24,25). The authors maintained their plants under laboratory conditions of 40% relative humidity, which may have enhanced the passive internalization of the virus, driven by increased transpiration rate of the plants under low relative humidity, as was shown for MNV in lettuce (39).…”

Section: Discussionmentioning

confidence: 99%

“…Internalization may also depend on the virus and the plant type, as TV at a low inoculum (10 4 GE/ml in 400 ml, i.e., 4 ϫ 10 6 GE/plant) or a high inoculum (10 6 GE/ml in 400 ml, i.e., 4 ϫ 10 8 in total feed water) was not detected in the leaves of green onions despite being detected in their roots (24). Furthermore, although washing the roots during the experimental setup may have caused minimal root damage and enhanced virus uptake, internalization of viruses in our study was not solely based on passive root uptake, as was evidenced by the different patterns of internalization for HuNoV and its surrogates SaV and TV.…”

Section: Discussionmentioning

confidence: 99%

“…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. 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.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Tissue Distribution and Visualization of Internalized Human Norovirus in Leafy Greens

Esseili

Meulia

Saif

et al. 2018

Appl Environ Microbiol

View full text Add to dashboard Cite

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.

show abstract

Internalization and dissemination of human norovirus and Tulane virus in fresh produce is plant dependent

Cited by 20 publications

References 51 publications

One Health for Food Safety, Food Security, and Sustainable Food Production

One Health for Food Safety, Food Security, and Sustainable Food Production

Selected Viruses Detected on and in our Food

Tissue Distribution and Visualization of Internalized Human Norovirus in Leafy Greens

Contact Info

Product

Resources

About