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

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

10.1101/2020.03.05.980078 ◽

2020 ◽

Author(s):

Neda Nasheri ◽

Jennifer Harlow ◽

Angela Chen ◽

Forest Dussault ◽

Nathalie Corneau ◽

...

Keyword(s):

Oxidative Process ◽

Foodborne Illnesses ◽

Foodborne Viruses ◽

Log Reduction ◽

Long Term Storage ◽

Viral Survival ◽

Low Moisture Foods ◽

Term Storage ◽

Advanced Oxidative Process

AbstractEnteric viruses, such as human norovirus (NoV) and hepatitis A virus (HAV), are the major causes of foodborne illnesses worldwide. These viruses are shed in high numbers, have low infectious dose, and may remain infectious for weeks in the environment and food. While numerous viral survival studies have been conducted in fresh fruits and produce, 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 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 long-term 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). 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 foodborne viruses can persist for 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% inactivation can be achieved for FCV, MNV, and HAV in chocolate, the inactivation efficiency diminishes to approximately 90% in pistachios and 70% in cereal. AOP treatment could therefore be a good candidate for the elimination of foodborne viruses from certain LMFs depending on the food matrix and surface of treatment.ImportanceLow moisture foods have been increasingly recognized as important vehicles of foodborne pathogens. In the present study, we demonstrated that foodborne viruses remain infectious during long-term storage on select low moisture foods. In addition, we evaluated the efficacy of an advanced oxidative process in the inactivation of foodborne viruses in low moisture foods. This research will help increase the safety of low moisture foods and reduce the number of foodborne illnesses due to contaminated products.

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Heat Inactivation of Hepatitis A Virus in Dairy Foods†

Journal of Food Protection ◽

10.4315/0362-028x-63.4.522 ◽

2000 ◽

Vol 63 (4) ◽

pp. 522-528 ◽

Cited By ~ 82

Author(s):

S. BIDAWID ◽

J. M. FARBER ◽

S. A. SATTAR ◽

S. HAYWARD

Keyword(s):

Dairy Products ◽

Hepatitis A ◽

Hepatitis A Virus ◽

Plaque Assay ◽

Virus Titer ◽

Skim Milk ◽

Fat Content ◽

Heat Inactivation ◽

Log Reduction ◽

Custom Made

Experiments were performed to determine the thermal resistance of hepatitis A virus (HAV) in three types of dairy products containing increased amounts of fat content (skim milk, homogenized milk; 3.5% MFG, and table cream; 18% MFG). HAV-inoculated dairy products were introduced into custom-made U-shaped microcapillary tubes that in turn were simultaneously immersed in a waterbath, using custom-made floating boats and a carrying platform. Following exposure to the desired time and temperature combinations, the contents of each of the tubes was retrieved and was tested by plaque assay to determine the reduction in virus titer. Our data indicated that <0.5 min at 85°C was sufficient to cause a 5-log reduction in HAV titer in all three dairy products, whereas at 80°C, ≤0.68 min (for skim and homogenized milk), and 1.24 min (for cream) were needed to cause a similar log reduction. Using a nonlinear two-phase negative exponential model (two-compartment model) to analyze the data, it was found that at temperatures of 65, 67, 69, 71, and 75°C, significantly (P < 0.05) higher exposure times were needed to achieve a 1-log reduction in virus titer in cream, as compared to skim and homogenized milk. For example, at 71°C, a significantly (P < 0.05) higher exposure time of 0.52 min (for cream) was needed as compared to ≤0.18 min (for skim and homogenized milk) to achieve a 1-log reduction in virus titer. A similar trend of inactivation was observed at 73 and 75°C where significantly (P < 0.05) higher exposure times of 0.29 to 0.36 min for cream were needed to cause a 1-log reduction in HAV in cream, as compared to ≤0.17 min for skim and homogenized milk. This study has provided information on the heat resistance of HAV in skim milk, homogenized milk, and table cream and demonstrated that an increase in fat content appears to play a protective role and contributes to the heat stability of HAV.

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Effect of Temperature and Relative Humidity on the Survival of Foodborne Viruses during Food Storage

Applied and Environmental Microbiology ◽

10.1128/aem.04093-14 ◽

2015 ◽

Vol 81 (6) ◽

pp. 2075-2081 ◽

Cited By ~ 22

Author(s):

Su Jin Lee ◽

Jiyeon Si ◽

Hyun Sun Yun ◽

GwangPyo Ko

Keyword(s):

Relative Humidity ◽

Survival Data ◽

Goodness Of Fit ◽

Hepatitis A Virus ◽

Plaque Assay ◽

Food Storage ◽

Effect Of Temperature ◽

Murine Norovirus ◽

Foodborne Viruses ◽

Biphasic Model

ABSTRACTMillions of people suffer from foodborne diseases throughout the world every year, and the importance of food safety has grown worldwide in recent years. The aim of this study was to investigate the survival of hepatitis A virus (HAV) and viral surrogates of human norovirus (HuNoV) (bacteriophage MS2 and murine norovirus [MNV]) in food over time. HAV, MNV, and MS2 were inoculated onto either the digestive gland of oysters or the surface of fresh peppers, and their survival on these food matrices was measured under various temperature (4°C, 15°C, 25°C, and 40°C) and relative humidity (RH) (50% and 70%) conditions. Inoculated viruses were recovered from food samples and quantified by a plaque assay at predetermined time points over 2 weeks (0, 1, 3, 7, 10, and 14 days). Virus survival was influenced primarily by temperature. On peppers at 40°C and at 50% RH, >4- and 6-log reductions of MNV and HAV, respectively, occurred within 1 day. All three viruses survived better on oysters. In addition, HAV survived better at 70% RH than at 50% RH. The survival data for HAV, MS2, and MNV were fit to three different mathematical models (linear, Weibull, and biphasic models). Among them, the biphasic model was optimum in terms of goodness of fit. The results of this study suggest that major foodborne viruses such as HAV and HuNoV can survive over prolonged periods of time with a limited reduction in numbers. Because a persistence of foodborne virus on contaminated foods was observed, precautionary preventive measures should be performed.

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Pressure Inactivation of Hepatitis A Virus in Strawberry Puree and Sliced Green Onions†

Journal of Food Protection ◽

10.4315/0362-028x-68.8.1748 ◽

2005 ◽

Vol 68 (8) ◽

pp. 1748-1751 ◽

Cited By ~ 69

Author(s):

DAVID H. KINGSLEY ◽

DONGSHENG GUAN ◽

DALLAS G. HOOVER

Keyword(s):

High Pressure ◽

Ambient Temperature ◽

Hepatitis A ◽

Hepatitis A Virus ◽

Intervention Strategy ◽

Plaque Assay ◽

High Pressure Processing

Hepatitis A can be acquired by ingesting contaminated produce. To investigate the potential of high-pressure processing as an intervention strategy for virus in produce, strawberry puree and sliced green onions were inoculated with >106 PFU of hepatitis A virus and treated with pressures ranging from 225 to 375 megapascals (MPa) in 25-MPa increments at ambient temperature. Subsequent virus extraction and plaque assay determined that hepatitis A virus was inactivated in strawberry puree and sliced green onions after 5-min exposures to pressures of 375 MPa with log PFU reductions of 4.32 and 4.75, respectively. Hepatitis A virus was equally sensitive in puree and onions at pressures ≥350 MPa. For treatments of <325 MPa, the virus was more sensitive to pressure in strawberry puree than in sliced onions with log reductions of 1.2, 2.06, and 3.13 observed for strawberries and 0.28, 0.72, and 1.42 observed for onions after 5-min treatments at 250, 275, and 300 MPa, respectively. Although high-pressure processing may cause some organoleptic alterations to strawberries and onions, results show high-pressure processing will inactivate hepatitis A virus in these foods.

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Evaluation of Bead-Based Assays for the Isolation of Foodborne Viruses from Low-Moisture Foods

Journal of Food Protection ◽

10.4315/0362-028x.jfp-19-345 ◽

2020 ◽

Vol 83 (3) ◽

pp. 388-396 ◽

Cited By ~ 2

Author(s):

NEDA NASHERI ◽

JENNIFER HARLOW ◽

ANGELA CHEN ◽

NATHALIE CORNEAU ◽

SABAH BIDAWID

Keyword(s):

Magnetic Beads ◽

Hepatitis A Virus ◽

Virus Transmission ◽

Magnetic Bead ◽

Murine Norovirus ◽

Foodborne Viruses ◽

Recovery Rates ◽

Porcine Gastric Mucin ◽

Low Moisture Foods ◽

Virus Recovery

ABSTRACT Foodborne viruses such as norovirus and hepatitis A virus (HAV) are highly transmissible, persistent in the environment, and resistant to many conventional inactivation methods. Foods can become contaminated with these viruses either at the source of harvest or during food handling and processing. Multiple lines of evidence suggest that foodborne viruses can survive desiccation and dry conditions. Several foodborne virus outbreaks have been linked to low-moisture foods (LMFs), indicating that these foods can be vehicles of virus transmission. However, the efficiencies of common virus extraction methodologies have not been examined with LMFs. We adapted the International Organization for Standardization (ISO) 15216-1:2017 method for virus recovery for use with chocolate, pistachios, and cornflakes. We also developed a magnetic bead assay for the recovery of HAV from LMFs and used the porcine gastric mucin–coated magnetic beads (PGM-MBs) to extract norovirus surrogates, feline calicivirus (FCV), and murine norovirus (MNV) from the same LMFs. The efficiency of virus recovery using the bead-based assay was then compared with that of the ISO 15216-1:2017 method. In chocolate and pistachios, the recovery rates with the PGM-MB method were 5.6- and 21.3-fold higher, respectively, for FCV and 1.65- and 18-fold higher, respectively, for MNV than those with the ISO 15216-1:2017 method. However, the PGM-MB method failed to recover MNV and FCV from cornflakes. The recovery rates for HAV in chocolate, pistachios, and corn flakes with the magnetic bead method were 11.5-, 3-, and 5.6-fold higher, respectively, than those with the ISO 15216-1:2017 method. Thus, depending upon the food matrix and the target virus, the bead-based assays can be used to efficiently and rapidly extract viruses from LMFs. HIGHLIGHTS

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Survival of Hepatitis A Virus on Two-month Stored Freeze-dried Berries

Journal of Food Protection ◽

10.4315/jfp-21-110 ◽

2021 ◽

Author(s):

Yan Zhang ◽

Xueyan Wang ◽

Y. Carol Shieh

Keyword(s):

Freeze Drying ◽

Hepatitis A ◽

Hepatitis A Virus ◽

Reduction Rate ◽

Radiant Heating ◽

Minimal Processing ◽

Log Reduction ◽

C Storage ◽

Freeze Dried ◽

Heating Up

Imported berries have contributed to U.S. hepatitis A virus (HAV) infections. Minimal processing by freeze-drying is preferred by industry for preserving food quality, but virus inactivation by this process may be limited. This study investigated HAV survival on strawberries during 24-h freeze-drying followed by 22 ° C-storage. The outer surfaces of strawberry slices were prepared and each inoculated with 5 to 6 log 10 PFU HAV, air-dried 20 min, frozen 1 h at -80 °C, and freeze-dried 24 h with radiant heating up to 36 °C. Infectious HAV levels eluted from berry slices were quantified on FRhK-4 cells grown onto 6-well dishes. Freeze-drying trials (n = 17) with radiant heating inactivated ≤1 log 10 PFU per trial, although HAV-inactivation was significantly greater at 36 ºC than 15 ºC heating ( p < 0.01). Average HAV reduction rate on dried berries continuously decreased as storage time increased, 0.2, 0.09, 0.08, 0.04, 0.04 and 0.03 log-reduction/day at day 2, 7, 14, 28, 42, and 56, respectively, with the cumulated log-reduction divided by storage days. Therefore, the best fit regression for the total/cumulative virus reduction (Y) at any given day (X) is Y= 0.2882X 0.4503 (r² = 0.97), with maximum 2.7 log-reduction on berries throughout the drying and subsequent 2-month storage. HAV showed the greatest decline within the first 14-days of storage of dried berries (approximately 70% weekly reduction from its previous week levels), but the HAV reduction rates were still lower than that occurring on fresh produce.

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Foodborne Transmission of Sars-Cov-2 Is More Evident Than It Has Been Before

10.20944/preprints202009.0361.v1 ◽

2020 ◽

Author(s):

Hamada Aboubakr ◽

Sagar Goyal

Keyword(s):

Infectious Virus ◽

Hepatitis A Virus ◽

Disease Outbreaks ◽

Foodborne Viruses ◽

Frozen Food ◽

Oral Transmission ◽

Viral Spread ◽

Food Packages ◽

Route Of Transmission ◽

The World

Background:Although highly strict social distancing and viral spread protection guidelines are in force, the reported numbers of COVID-19 cases across the world are still increasing. This indicates that we are still unable to completely understand the transmission routes of SARS-CoV-2. One of the possible routes that can play a significant role is the fecal-oral transmission since SARS-CoV-2 can replicate in the intestines as demonstrated by isolation of infectious virus from fecal samples of COVID-19 cases. Scope and approach:In this review, we compare the characteristics of SARS-CoV-2 with the distinctive characteristics of enteric foodborne viruses. We also discuss and respond to the arguments given in some reports that downplay the importance of foodborne transmission route of SARS-CoV-2. Key findings and conclusions:Enteric viruses such as human noroviruses (HuNoVs) and hepatitis A virus (HAV) are known to transmit through foods such as fresh produce and berries, leading to frequent multistate foodborne disease outbreaks all over the world. SARS-CoV-2 was found to share four distinctive characteristics of foodborne viruses that allow them to transmit through foods. This similarity in characteristics, recent report of detecting SARS-CoV-2 particles from frozen food packages in China, and recent suspected foodborne COVID-19 case in New Zealand, indicate that foodborne transmission of SARS-CoV-2 is more evident than previously thought possible. To support or deny this route of transmission, urgent research needs to be undertaken to answer two primary questions and many secondary ones as described in this review.

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Incidence of hepatitis A and hepatitis E viruses and norovirus and rotavirus in fish and shrimp samples caught from the Persian Gulf

Arquivo Brasileiro de Medicina Veterinária e Zootecnia ◽

10.1590/1678-4162-11742 ◽

2021 ◽

Vol 73 (1) ◽

pp. 169-178

Author(s):

M. Alipour Amroabadi ◽

E. Rahimi ◽

A. Shakerian ◽

H. Momtaz

Keyword(s):

Persian Gulf ◽

Hepatitis E Virus ◽

Hepatitis A ◽

Hepatitis A Virus ◽

Penaeus Monodon ◽

Hepatitis E ◽

Foodborne Viruses ◽

Scomberomorus Commerson ◽

The Persian Gulf ◽

Autumn And Winter

ABSTRACT Foodborne viruses including hepatitis A virus (HAV), norovirus (NoV), rotavirus (RoV) and hepatitis E virus (HEV) are easily transmitted through contaminated seafoods. The current research was done to assess the incidence of RoV, NoV GI and GII,hAV and hEV in fish and shrimp samples caught from the Persian Gulf, Iran. Three-hundred and twenty fish and shrimp samples were collected. The presence of foodborne viruses were assessed by the real-time PCR. Forty-nine out of 320 (15.31%) fish and shrimp samples were positive for foodborne viruses. Distribution of hAV, NoV GI and NoV GII amongst all studied samples were 0.93%, 5.93% and 8.43%, respectively. hEV and RoV viruses were not found in studied samples. Parastromateus niger and Scomberomorus commerson fish and Penaeus monodon shrimp were the most frequently contaminated samples. Simultaneous incidence of hAV and NoV GI and hAV and NoV GII were 0.31% and 0.93%, respectively. Distribution of foodborne viruses in samples collected through spring, summer, autumn and winter seasons were 14.28%, 9.33%, 11.76% and 24.44%, respectively. Findings revealed that the incidence of foodborne viruses was significantly associated with seafood species and also season of sampling.

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Survival of Hepatitis A Virus in Spinach during Low Temperature Storage

Journal of Food Protection ◽

10.4315/0362-028x-72.11.2390 ◽

2009 ◽

Vol 72 (11) ◽

pp. 2390-2393 ◽

Cited By ~ 27

Author(s):

Y. CAROL SHIEH ◽

DIANA S. STEWART ◽

DAVID T. LAIRD

Keyword(s):

Hepatitis A ◽

Hepatitis A Virus ◽

Plaque Assay ◽

Storage Conditions ◽

Inactivation Rate ◽

Low Temperature Storage ◽

Foodborne Outbreaks ◽

Phosphate Buffered Saline ◽

Temperature Storage ◽

Spinach Leaves

Spinach leaves are frequently consumed raw and have been involved with past foodborne outbreaks. In this study, we examined the survival of hepatitis A virus (HAV) on fresh spinach leaves in moisture- and gas-permeable packages that were stored at 5.4 ± 1.2°C for up to 42 days. Different eluents including phosphate-buffered saline (PBS), pH 7.5 (with and without 2% serum), and 3% beef extract (pH 7.5 and 8) were compared for how efficiently they recovered viruses from spinach by using a simple elution procedure (<1 h). The recoveries were compared and determined by a plaque assay with FRhK-4 cells. Culture grade PBS containing 2% serum was found to be appropriate for HAV elution from spinach leaves, with an average recovery of 45% ± 10%. Over 4 weeks of storage at 5.4 ± 1.2°C, HAV in spinach decreased slightly more than 1 log, with 6.75% of the original titer remaining. HAV survived under refrigerated temperatures on spinach leaves with a D-value of 28.6 days (equivalent to an inactivation rate of 20.035 log of HAV per day, r2 = 0.88). In comparison, HAV in PBS containing 2% serum under the same storage conditions remained constant throughout 7 weeks. The inactivation rate of 20.035 log each day for HAV on spinach leaves was possibly due to the interaction of the virus and the leaf.

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