Human Norovirus Surrogate Is Highly Stable in Berry Smoothies and Under In Vitro Simulated Digestion

Overview

Journal Foods

Specialty Biotechnology

Date 2024 Apr 13

PMID 38611370

Authors

Riya Hooda

Malak A Esseili

Affiliations

Soon will be listed here.

Abstract

Human noroviruses are major causes of foodborne outbreaks linked to berries. The overall goal of this study was to investigate the persistence of a human norovirus surrogate, Tulane virus (TV), in berry smoothies and under simulated digestion through the gastrointestinal track. Two types of smoothies were prepared from blueberries and strawberries. Tulane virus was spiked into each smoothie and incubated either at 37 or 4 °C for 2, 60, and 120 min. Furthermore, the virus-spiked smoothies were subjected to sequential oral (2 min), gastric (10 and 60 min), and intestinal (15 and 120 min) digestion according to the standardized INFOGEST model. Quantification of infectious TV was carried out using the TCID assay. At 4 °C, in both berry smoothies, TV infectivity did not show significant changes throughout the 120 min period. At 37 °C, TV infectivity showed significant reduction (~0.5 log TCID/mL) only in blueberry smoothies starting at 60 min. During the oral, gastric, and intestinal digestion phases, the mean log reduction in TV infectivity in blueberry did not exceed ~0.5 log, while infectious TV in strawberry smoothies under all phases was stable. Given the notable stability of infectious viruses in berry smoothies and the gastrointestinal tract, prevention of norovirus contamination of berries is paramount to reduce virus outbreaks linked to berries.

References

Esseili M, Gao X, Tegtmeier S, Saif L, Wang Q . Abiotic Stress and Phyllosphere Bacteria Influence the Survival of Human Norovirus and Its Surrogates on Preharvest Leafy Greens. Appl Environ Microbiol. 2015; 82(1):352-63. PMC: 4702653. DOI: 10.1128/AEM.02763-15. View

Macori G, Gilardi G, Bellio A, Bianchi D, Gallina S, Vitale N . Microbiological Parameters in the Primary Production of Berries: A Pilot Study. Foods. 2018; 7(7). PMC: 6069088. DOI: 10.3390/foods7070105. View

Esseili M, Mann A, Narwankar R, Kassem I, Diez-Gonzalez F, Hogan R . SARS-CoV-2 remains infectious for at least a month on artificially-contaminated frozen berries. Food Microbiol. 2022; 107:104084. PMC: 9214230. DOI: 10.1016/j.fm.2022.104084. View

Zang R, Gomez Castro M, McCune B, Zeng Q, Rothlauf P, Sonnek N . TMPRSS2 and TMPRSS4 promote SARS-CoV-2 infection of human small intestinal enterocytes. Sci Immunol. 2020; 5(47). PMC: 7285829. DOI: 10.1126/sciimmunol.abc3582. View

Lee E, Han S, Hyun S, Song G, Ha S . Survival of human coronavirus 229E at different temperatures on various food-contact surfaces and food and under simulated digestive conditions. Food Res Int. 2022; 162(Pt A):112014. PMC: 9526873. DOI: 10.1016/j.foodres.2022.112014. View

Verhaelen K, Bouwknegt M, Lodder-Verschoor F, Rutjes S, de Roda Husman A . Persistence of human norovirus GII.4 and GI.4, murine norovirus, and human adenovirus on soft berries as compared with PBS at commonly applied storage conditions. Int J Food Microbiol. 2012; 160(2):137-44. DOI: 10.1016/j.ijfoodmicro.2012.10.008. View

Esseili M, Meulia T, Saif L, Wang Q . Tissue Distribution and Visualization of Internalized Human Norovirus in Leafy Greens. Appl Environ Microbiol. 2018; 84(12). PMC: 5981073. DOI: 10.1128/AEM.00292-18. View

Hall A, Wikswo M, Pringle K, Gould L, Parashar U . Vital signs: foodborne norovirus outbreaks - United States, 2009-2012. MMWR Morb Mortal Wkly Rep. 2014; 63(22):491-5. PMC: 5779359. View

Falco I, Randazzo W, Rodriguez-Diaz J, Gozalbo-Rovira R, Luque D, Aznar R . Antiviral activity of aged green tea extract in model food systems and under gastric conditions. Int J Food Microbiol. 2018; 292:101-106. DOI: 10.1016/j.ijfoodmicro.2018.12.019. View

10.

Bozkurt H, Phan-Thien K, van Ogtrop F, Bell T, McConchie R . Outbreaks, occurrence, and control of norovirus and hepatitis a virus contamination in berries: A review. Crit Rev Food Sci Nutr. 2020; 61(1):116-138. DOI: 10.1080/10408398.2020.1719383. View

11.

Souza V, Pereira P, da Silva T, Lima L, Pio R, Queiroz F . Determination of the bioactive compounds, antioxidant activity and chemical composition of Brazilian blackberry, red raspberry, strawberry, blueberry and sweet cherry fruits. Food Chem. 2014; 156:362-8. DOI: 10.1016/j.foodchem.2014.01.125. View

12.

Joshi S, Howell A, DSouza D . Reduction of Enteric Viruses by Blueberry Juice and Blueberry Proanthocyanidins. Food Environ Virol. 2016; 8(4):235-243. DOI: 10.1007/s12560-016-9247-3. View

13.

Tian P, Yang D, Quigley C, Chou M, Jiang X . Inactivation of the Tulane virus, a novel surrogate for the human norovirus. J Food Prot. 2013; 76(4):712-8. PMC: 4073237. DOI: 10.4315/0362-028X.JFP-12-361. View

14.

Mercanoglu Taban B, Halkman A . Do leafy green vegetables and their ready-to-eat [RTE] salads carry a risk of foodborne pathogens?. Anaerobe. 2011; 17(6):286-7. DOI: 10.1016/j.anaerobe.2011.04.004. View

15.

Lopman B, Steele D, Kirkwood C, Parashar U . The Vast and Varied Global Burden of Norovirus: Prospects for Prevention and Control. PLoS Med. 2016; 13(4):e1001999. PMC: 4846155. DOI: 10.1371/journal.pmed.1001999. View

16.

LeBlanc D, Gagne M, Poitras E, Brassard J . Persistence of murine norovirus, bovine rotavirus, and hepatitis A virus on stainless steel surfaces, in spring water, and on blueberries. Food Microbiol. 2019; 84:103257. DOI: 10.1016/j.fm.2019.103257. View

17.

Zivkovic I, Savikin K, Zivkovic J, Zdunic G, Jankovic T, Lazic D . Antiviral Effects of Pomegranate Peel Extracts on Human Norovirus in Food Models and Simulated Gastrointestinal Fluids. Plant Foods Hum Nutr. 2021; 76(2):203-209. PMC: 8024177. DOI: 10.1007/s11130-021-00895-7. View

18.

Hoffmann S, Batz M, Morris Jr J . Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J Food Prot. 2012; 75(7):1292-302. DOI: 10.4315/0362-028X.JFP-11-417. View

19.

Miller K, Feucht W, Schmid M . Bioactive Compounds of Strawberry and Blueberry and Their Potential Health Effects Based on Human Intervention Studies: A Brief Overview. Nutrients. 2019; 11(7). PMC: 6683271. DOI: 10.3390/nu11071510. View

20.

Gil M, Selma M, Suslow T, Jacxsens L, Uyttendaele M, Allende A . Pre- and postharvest preventive measures and intervention strategies to control microbial food safety hazards of fresh leafy vegetables. Crit Rev Food Sci Nutr. 2014; 55(4):453-68. DOI: 10.1080/10408398.2012.657808. View