Attachment and localization of human norovirus and animal caliciviruses in fresh produce

DiCaprio, Erin; Purgianto, Anastasia; Ma, Yuanmei; Hughes, John H.; Dai, Xianzhong; Lǐ, Jiànróng

doi:10.1016/j.ijfoodmicro.2015.07.013

Cited by 28 publications

(16 citation statements)

References 31 publications

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“…Washing of fresh produce may prove ineffective to remove microorganisms, as they may remain attached to plant surfaces (DiCaprio et al, 2015), or become internalized in the edible parts of the plant (Franz & van Bruggen, 2008), and thus, are not accessible for efficient removal. In addition, the water used to wash fresh produce can be a source of microbial contamination (CDC, 1989;Hedberg et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Microbial Contamination of Fresh Produce: What, Where, and How?

Machado-Moreira

Richards

Brennan

et al. 2019

Comp Rev Food Sci Food Safe

185

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Promotion of healthier lifestyles has led to an increase in consumption of fresh produce. Such foodstuffs may expose consumers to increased risk of foodborne disease, as often they are not subjected to processing steps to ensure effective removal or inactivation of pathogenic microorganisms before consumption. Consequently, reports of ready‐to‐eat fruit and vegetable related disease outbreak occurrences have increased substantially in recent years, and information regarding these events is often not readily available. Identifying the nature and source of microbial contamination of these foodstuffs is critical for developing appropriate mitigation measures to be implemented by food producers. This review aimed to identify the foodstuffs most susceptible to microbial contamination and the microorganisms responsible for disease outbreaks from information available in peer‐reviewed scientific publications. A total of 571 outbreaks were identified from 1980 to 2016, accounting for 72,855 infections and 173 deaths. Contaminated leafy green vegetables were responsible for 51.7% of reported outbreaks. Contaminated soft fruits caused 27.8% of infections. Pathogenic strains of Escherichia coli and Salmonella, norovirus, and hepatitis A accounted for the majority of cases. Large outbreaks resulted in particular biases such as the observation that contaminated sprouted plants caused 31.8% of deaths. Where known, contamination mainly occurred via contaminated seeds, water, and contaminated food handlers. There is a critical need for standardized datasets regarding all aspects of disease outbreaks, including how foodstuffs are contaminated with pathogenic microorganisms. Providing food business operators with this knowledge will allow them to implement better strategies to improve safety and quality of fresh produce.

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Section: Introductionmentioning

confidence: 99%

Microbial Contamination of Fresh Produce: What, Where, and How?

Machado-Moreira

Richards

Brennan

et al. 2019

Comp Rev Food Sci Food Safe

185

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“…A recent study has shown that HuNoV VLP, TV, and MNV preferentially aggregate inside lettuce stomata, suggesting that the three viruses exhibit similar patterns of attachment to lettuce leaves (53). However, specific binding was not investigated in that study.…”

Section: Discussionmentioning

confidence: 89%

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

Esseili

Gao

Tegtmeier

et al. 2016

Appl Environ Microbiol

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Foodborne outbreaks of human noroviruses (HuNoVs) are frequently associated with leafy greens. Because there is no effective method to eliminate HuNoV from postharvest leafy greens, understanding virus survival under preharvest conditions is crucial. The objective of this study was to evaluate the survival of HuNoV and its surrogate viruses, murine norovirus (MNV), porcine sapovirus (SaV), and Tulane virus (TV), on preharvest lettuce and spinach that were subjected to abiotic stress (physical damage, heat, or flood). We also examined the bacteria culturable from the phyllosphere in response to abiotic stress and in relation to viral persistence. Mature plants were subjected to stressors 2 days prior to inoculation of the viruses on leaves. We quantified the viral RNA, determined the infectivity of the surrogates, and performed bacterial counts on postinoculation days (PIDs) 0, 1, 7, and 14. For both plant types, time exerted significant effects on HuNoV, MNV, SaV, and TV RNA titers, with greater effects being seen for the surrogates. Infectious surrogate viruses were undetectable on PID 14. Only physical damage on PID 14 significantly enhanced HuNoV RNA persistence on lettuce, while the three stressors differentially enhanced the persistence of MNV and TV RNA. Bacterial counts were significantly affected by time and plant type but not by the stressors. However, bacterial counts correlated significantly with HuNoV RNA titers on spinach and with the presence of surrogate viruses on both plant types under various conditions. In conclusion, abiotic stressors and phyllosphere bacterial density may differentially influence the survival of HuNoV and its surrogates on lettuce and spinach, emphasizing the need for the use of preventive measures at the preharvest stage.H uman noroviruses (HuNoVs) are the leading cause of acute gastroenteritis and foodborne illnesses in the United States, causing 19 million to 21 million cases, 570 to 800 deaths, and $777 million in health care-associated costs annually (1). These singlestranded RNA viruses belong to the Caliciviridae family and are 28 to 35 nm in diameter and nonenveloped. Although these viruses cause self-limiting gastroenteritis, more serious infections can develop in high-risk groups, such as the elderly and immunocompromised populations (2). The virus is mainly transmitted to humans via the fecal-oral route either by contact with an infected person or fomites or by ingestion of contaminated food and water (2). Leafy greens are frequently associated with HuNoV outbreaks (1) and are globally recognized to be a high priority in terms of the microbial safety of fresh produce (3). Contamination of leafy greens with HuNoVs can occur at any stage along the farm-to-fork chain (3) through a number of sources, including fecally contaminated water used for irrigation, improperly treated sewage sludge used for fertilization, and food harvesters or food handlers who use improper hygiene practices (4, 5). Because HuNoVs have a low infectious dose (ϳ18 to 1,000 viral particles) (6) ...

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“…After viruses attach to the surface of lettuce cell wall they bind by multiple carbohydrate moieties and electrostatic force may play a major role in controlling virus adsorption and enhance virus persistence on the leaf surface. 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].…”

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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Attachment and localization of human norovirus and animal caliciviruses in fresh produce

Cited by 28 publications

References 31 publications

Microbial Contamination of Fresh Produce: What, Where, and How?

Microbial Contamination of Fresh Produce: What, Where, and How?

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

Noroviruses in food chain production

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