Foodborne viral outbreaks associated with frozen produce

Nasheri, Neda; Vester, Adrian; Petronella, Nicholas

doi:10.1017/s0950268819001791

Cited by 48 publications

(25 citation statements)

References 57 publications

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“…For this reason, minimal intervention strategies are implemented during the production of LMFs (Sanchez-Maldonado et al 2018 ). However, foodborne viruses are relatively resistant to various environmental factors (e.g., pH, temperature, and a w ), and viral persistence in various environments, such as food surfaces and soil, has been demonstrated (Rzezutka and Cook 2004 ; Nasheri et al 2019 ; Yeargin and Gibson 2018 ). Following the contamination of food and food surfaces with foodborne viruses through different mechanisms such as infected food-handlers, contamination with sewage (Shukla et al 2018 ), the virus can remain infectious for a relatively long time (Cook et al 2018 , 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Survival and Inactivation by Advanced Oxidative Process of Foodborne Viruses in Model Low-Moisture Foods

Nasheri

Harlow²,

Chen³

et al. 2021

Food Environ Virol

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Enteric viruses, such as human norovirus (NoV) and hepatitis A virus (HAV), are the major causes of foodborne illnesses worldwide. These viruses have low infectious dose, and may remain infectious for weeks in the environment and food. Limited information is available regarding viral survival and transmission in low-moisture foods (LMF). LMFs are generally considered as ready-to-eat products, which undergo no or minimal pathogen reduction steps. However, numerous foodborne viral outbreaks associated with LMFs have been reported in recent years. The objective of this study was to examine the survival of foodborne viruses in LMFs during 4-week storage at ambient temperature and to evaluate the efficacy of advanced oxidative process (AOP) treatment in the inactivation of these viruses. For this purpose, select LMFs such as pistachios, chocolate, and cereal were inoculated with HAV and the norovirus surrogates, murine norovirus (MNV) and feline calicivirus (FCV), then viral survival on these food matrices was measured over a four-week incubation at ambient temperature, by both plaque assay and droplet-digital RT-PCR (ddRT-PCR) using the modified ISO-15216 method as well as the magnetic bead assay for viral recovery. We observed an approximately 0.5 log reduction in viral genome copies, and 1 log reduction in viral infectivity for all three tested viruses following storage of select inoculated LMFs for 4 weeks. Therefore, the present study shows that the examined foodborne viruses can persist for a long time in LMFs. Next, we examined the inactivation efficacy of AOP treatment, which combines UV-C, ozone, and hydrogen peroxide vapor, and observed that while approximately 100% (4 log) inactivation can be achieved for FCV, and MNV in chocolate, the inactivation efficiency diminishes to approximately 90% (1 log) in pistachios and 70% (< 1 log) in cereal. AOP treatment could therefore be a good candidate for risk reduction of foodborne viruses from certain LMFs depending on the food matrix and surface of treatment.

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Section: Introductionmentioning

confidence: 99%

Survival and Inactivation by Advanced Oxidative Process of Foodborne Viruses in Model Low-Moisture Foods

Nasheri

Harlow²,

Chen³

et al. 2021

Food Environ Virol

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“…This needs to be taken into consideration, given that frozen berries can be stored for long periods by distributors and subsequently by consumers ( Hutin et al, 1999 ; Collier et al, 2014 ; Müller et al, 2015 ). For this reason, frozen berries have been implicated on numerous occasions in outbreaks of foodborne viral gastroenteritis and are closely monitored by government agencies (reviewed by Tavoschi et al, 2015 ; Nasheri et al, 2019 ). Regardless of the variety of treatments used to reduce the infectious viral load on the surfaces of frozen produce, our results suggest that residual inactivated virus may persist for several months at low temperatures, and its detection could be interpreted as the presence of infectious virus.…”

Section: Discussionmentioning

confidence: 99%

“…Other contamination routes are sewage-polluted irrigation water and fishing sites ( Kokkinos et al, 2012 ; Lopman et al, 2012 ; Verhaelen et al, 2013 ; Randazzo and Sánchez, 2020 ). Leafy vegetables, such as lettuce, mixed salads, and green onions, are the most frequently contaminated vegetables ( Wheeler et al, 2005 ; Herman et al, 2015 ), whereas berries are frequently contaminated fruits ( Chatziprodromidou et al, 2018 ; Nasheri et al, 2019 ). Enteric viruses can remain infectious under harsh environmental conditions, and imported frozen fruits have been involved in recent outbreaks in industrialized countries ( Bernard et al, 2014 ; Collier et al, 2014 ; Severi et al, 2015 ; Franklin et al, 2019 ; Nasheri et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

“…Leafy vegetables, such as lettuce, mixed salads, and green onions, are the most frequently contaminated vegetables ( Wheeler et al, 2005 ; Herman et al, 2015 ), whereas berries are frequently contaminated fruits ( Chatziprodromidou et al, 2018 ; Nasheri et al, 2019 ). Enteric viruses can remain infectious under harsh environmental conditions, and imported frozen fruits have been involved in recent outbreaks in industrialized countries ( Bernard et al, 2014 ; Collier et al, 2014 ; Severi et al, 2015 ; Franklin et al, 2019 ; Nasheri et al, 2019 ). This has led governmental bodies such as the U.S. Food and Drug Administration and the Canadian Food Inspection Agency to establish surveillance plans for viruses in fresh and frozen fruits ( Canadian Food Inspection Agency, 2017 ; U.S. Food and Drug Administration, 2020a ).…”

Section: Introductionmentioning

confidence: 99%

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Persistence of Hepatitis A Virus RNA in Water, on Non-porous Surfaces, and on Blueberries

2021

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Enteric viruses, such as human norovirus and hepatitis A virus (HAV), are the leading cause of transmissible foodborne illness. Fresh produce such as berries are often contaminated by infected food handlers, soiled water, or food contact surfaces. The gold-standard method for virus detection throughout the food chain is RT-qPCR, which detects portions of genomes including non-infectious viral particles and naked viral RNA. The aim of this study was to evaluate the persistence of heat-inactivated HAV in water, phosphate-buffered saline, on stainless steel and polyvinyl chloride, and on blueberries at −80°C, −20°C, 4°C, and room temperature. In water and phosphate-buffered saline, viral RNA could be detected for up to 90 days regardless of temperature when the initial load was 2.5 × 104 or 2.5 × 106 genome copies. It was detected on polyvinyl chloride and blueberries under most conditions. On stainless steel, the large initial load persisted for 90 days, while the medium-level load was detected only up to 16 days at room temperature or 60 days at 4°C. The detection of non-infectious viral RNA can confound investigations of gastroenteritis outbreaks. Pretreatments that discriminate between naked RNA, non-infectious virions and infectious virions need to be included in the RT-qPCR method in order to reduce the risk of positive results associated with non-infectious viral particles.

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“…Chemical, sensory and microbiological parameters of products improve after GMP training and applications (Ramón et al, 2018). Although HACCP and GMP implemented in the majority of food facilities, recently foodborne outbreaks and diseases related with frozen industry have raised in global public health concern (Nasheri et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Monitoring environmental microbiological safety in a frozen fruit and vegetable plant

Çinar

Onbaşı

2021

Food Sci. Technol

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Ensuring food safety is becoming progressively important in frozen foods due to increased demand and consumption worldwide. The Environmental Monitoring Program (EMP) shall support daily operational activities and monitor the lack of process hygiene & sanitation actions to achieve food safety. The aim of this study was implementation of EMP in the frozen fruit and vegetable factory to identify the place that allows for pathogen/indicator microorganism growth and create preventive actions to reduce or eliminate the risk of cross-contamination. A total of 400 swab samples, Zone 1 (n = 228), Zone 2 (n = 90), Zone 3 (n = 52), Zone 4 (n = 30) were examined for E. coli and Coliform, Total Plate Count (TPC), yeast and mold and environmental Listeria spp. The percentage of satisfying target value before vs after the implementation of EMP was 82% vs. 100% for E. coli, 61% vs. 86% for Coliforms, 48% vs. 77% for TPC and 63% vs. 80% for yeast & mold respectively for Zone 1. Environmental Listeria was not determined in any of the zones. Integration of EMP to food safety management systems is essential to prevent outbreaks, recalls and economic losses. In addition to depending on the developing technologies, EMP should be supported with new corrective actions.

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Foodborne viral outbreaks associated with frozen produce

Cited by 48 publications

References 57 publications

Survival and Inactivation by Advanced Oxidative Process of Foodborne Viruses in Model Low-Moisture Foods

Survival and Inactivation by Advanced Oxidative Process of Foodborne Viruses in Model Low-Moisture Foods

Persistence of Hepatitis A Virus RNA in Water, on Non-porous Surfaces, and on Blueberries

Monitoring environmental microbiological safety in a frozen fruit and vegetable plant

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