Abstract
Human norovirus (HuNoV) is a pathogenic agent that is frequently associated with foodborne disease outbreaks linked to fresh produce. Within microgreen production systems, understanding of virus transmission routes and persistence is limited. To investigate virus persistence on microgreen leaf surfaces, this study mimicked virus contaminations caused during microgreen handling by farm workers or during overhead irrigation with contaminated water. Specifically, approximately 5 log PFU of Tulane virus (TV)—a HuNoV surrogate—was inoculated on sunflower (SF) and pea shoot (PS) microgreen leaves at 7-day age. The virus reduction on SF was significantly higher than PS (p < 0.05). On day 10, total TV reduction for SF and PS were 3.70 ± 0.10 and 2.52 ± 0.30 log PFU/plant, respectively. Under the environmental scanning electron microscope (ESEM) observation, the leaf surfaces of SF were visually smoother than PS, while their specific effect on virus persistence were not further characterized. Overall, this study revealed that TV persistence on microgreen leaves was plant variety dependent. In addition, this study provided a preliminary estimation on the risk of HuNoV contamination in a microgreen production system which will aim the future development of prevention and control measures.
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Arthur, S. E., & Gibson, K. E. (2015). Physicochemical stability profile of Tulane virus: A human norovirus surrogate. Journal of Applied Microbiology, 119(3), 868–875. https://doi.org/10.1111/jam.12878
Bosch, A., Gkogka, E., Le Guyader, F. S., Loisy-Hamon, F., Lee, A., van Lieshout, L., et al. (2018). Foodborne viruses: Detection, risk assessment, and control options in food processing. International Journal of Food Microbiology, 285, 110–128. https://doi.org/10.1016/j.ijfoodmicro.2018.06.001
Centers for Disease Control and Prevention. (2016). Types of Agricultural Water Use | Other Uses of Water | Healthy Water | CDC. https://www.cdc.gov/healthywater/other/agricultural/types.html. Accessed 8 July 2021.
Chatziprodromidou, I. P., Bellou, M., Vantarakis, G., & Vantarakis, A. (2018). Viral outbreaks linked to fresh produce consumption: A systematic review. Journal of Applied Microbiology, 124(4), 932–942. https://doi.org/10.1111/jam.13747
Cook, N., Knight, A., & Richards, G. P. (2016). Persistence and elimination of human norovirus in food and on food contact surfaces: A critical review. Journal of Food Protection, 79(7), 1273–1294. https://doi.org/10.4315/0362-028X.JFP-15-570
Di Gioia, F., Renna, M., & Santamaria, P. (2017). Sprouts, microgreens and “Baby Leaf” vegetables. In F. Yildiz & R. C. Wiley (Eds.), Minimally Processed refrigerated fruits and vegetables (pp. 403–432). Boston, MA: Springer.
Doan, H. K., Antequera-Gómez, M. L., Parikh, A. N., & Leveau, J. H. J. (2020a). Leaf surface topography contributes to the ability of Escherichia coli on leafy greens to resist removal by washing, escape disinfection with chlorine, and disperse through splash. Frontiers in Microbiology,. https://doi.org/10.3389/fmicb.2020.01485
Doan, H. K., Ngassam, V. N., Gilmore, S. F., Tecon, R., Parikh, A. N., & Leveau, J. H. J. (2020b). Topography-driven shape, spread, and retention of leaf surface water impacts microbial dispersion and activity in the phyllosphere. Phytobiomes Journal, 4(3), 268–280. https://doi.org/10.1094/PBIOMES-01-20-0006-R
Drouaz, N., Schaeffer, J., Farkas, T., Pendu, J. L., & Guyader, F. S. L. (2015). Tulane virus as a potential surrogate to mimic norovirus behavior in oysters. Applied and Environmental Microbiology, 81(15), 5249–5256. https://doi.org/10.1128/AEM.01067-15
Ebert, A. W. (2022). Sprouts and microgreens—novel food sources for healthy diets. Plants, 11(4), 571. https://doi.org/10.3390/plants11040571
Esseili, M. A., Gao, X., Boley, P., Hou, Y., Saif, L. J., Brewer-Jensen, P., et al. (2019). Human Norovirus Histo-Blood Group Antigen (HBGA) Binding Sites Mediate the Virus Specific Interactions with Lettuce Carbohydrates. Viruses. https://doi.org/10.3390/v11090833
Esseili, M. A., Gao, X., Tegtmeier, S., Saif, L. J., & Wang, Q. (2016). Abiotic stress and phyllosphere bacteria influence the survival of human norovirus and its surrogates on preharvest leafy greens. Applied and Environmental Microbiology, 82(1), 352–363. https://doi.org/10.1128/AEM.02763-15
Esseili, M. A., Wang, Q., & Saif, L. J. (2012). Binding of Human GII.4 norovirus virus-like particles to carbohydrates of romaine lettuce leaf cell wall materials. Applied and Environmental Microbiology, 78(3), 786–794. https://doi.org/10.1128/AEM.07081-11
Galieni, A., Falcinelli, B., Stagnari, F., Datti, A., & Benincasa, P. (2020). Sprouts and microgreens: Trends, opportunities, and horizons for novel research. Agronomy, 10(9), 1424.https://doi.org/10.3390/agronomy10091424
Healthy Canadians. (2020). Picoudi brand microgreens recalled due to Salmonella. https://healthycanadians.gc.ca/recall-alert-rappel-avis/inspection/2020/73833r-eng.php. Accessed 8 July 2021.
Healthy Canadians. (2021). Certain Broadwood Farm brand microgreens recalled due to Salmonella—Recalls, advisories and safety alerts – Canada.ca. Government of Canada, Health Canada, CFIA. https://recalls-rappels.canada.ca/en/alert-recall/certain-broadwood-farm-brand-microgreens-recalled-due-salmonella. Accessed 26 May 2022.
Hirneisen, K. A., & Kniel, K. E. (2013). Norovirus surrogate survival on spinach during preharvest growth. Phytopathology, 103(4), 389–394. https://doi.org/10.1094/PHYTO-09-12-0231-FI
Jung, Y., Jang, H., & Matthews, K. R. (2014). Effect of the food production chain from farm practices to vegetable processing on outbreak incidence. Microbial Biotechnology, 7(6), 517–527. https://doi.org/10.1111/1751-7915.12178
Kroupitski, Y., Golberg, D., Belausov, E., Pinto, R., Swartzberg, D., Granot, D., & Sela, S. (2009). Internalization of salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Applied and Environmental Microbiology, 75(19), 6076–6086. https://doi.org/10.1128/AEM.01084-09
Li, D., & Uyttendaele, M. (2018). Potential of Human norovirus surrogates and salmonella enterica contamination of pre-harvest Basil (Ocimum basilicum) via leaf surface and plant substrate. Frontiers in Microbiology,. https://doi.org/10.3389/fmicb.2018.01728
Lima, P. M., São José, J. F. B., Andrade, N. J., Pires, A. C. S., & Ferreira, S. O. (2013). Interaction between natural microbiota and physicochemical characteristics of lettuce surfaces can influence the attachment of Salmonella Enteritidis. Food Control, 30(1), 157–161. https://doi.org/10.1016/j.foodcont.2012.06.039
Macarisin, D., Patel, J., Bauchan, G., Giron, J. A., & Ravishankar, S. (2013). Effect of spinach cultivar and bacterial adherence factors on survival of Escherichia coli O157:H7 on spinach leaves. Journal of Food Protection, 76(11), 1829–1837. https://doi.org/10.4315/0362-028X.JFP-12-556
Machado-Moreira, B., Richards, K., Brennan, F., Abram, F., & Burgess, C. M. (2019). Microbial contamination of fresh produce: What, where, and how? Comprehensive Reviews in Food Science and Food Safety, 18(6), 1727–1750. https://doi.org/10.1111/1541-4337.12487
Misra, G., & Gibson, K. E. (2021). Characterization of microgreen growing operations and associated food safety practices. Food Protection Trends, 41(1), 56–69.
Murray, K., Wu, F., Shi, J., Jun Xue, S., & Warriner, K. (2017). Challenges in the microbiological food safety of fresh produce: Limitations of post-harvest washing and the need for alternative interventions. Food Quality and Safety, 1(4), 289–301. https://doi.org/10.1093/fqsafe/fyx027
Park, H. K., Kushad, M. M., & Feng, H. (2013). Survival of Escherichia coli O157:H7 87:23 on Arugula, Kale, Lettuce and Mizuna Microgreens, and Comparison of Leaf Surface Morphology for Mature Greens and Microgreens. Charlotte, NC.
Renna, M., & Paradiso, V. M. (2020). Ongoing research on microgreens: nutritional properties, shelf-life, sustainable production, innovative growing and processing approaches. Foods. https://doi.org/10.3390/foods9060826
Rowe, H. C., Ro, D., & Rieseberg, L. H. (2012). Response of Sunflower (Helianthus annuus L.) Leaf Surface Defenses to Exogenous Methyl Jasmonate. PLoS ONE, 7(5), e37191. https://doi.org/10.1371/journal.pone.0037191
Steele, M., & Odumeru, J. (2004). Irrigation water as source of foodborne pathogens on fruit and vegetables. Journal of Food Protection, 67(12), 2839–2849. https://doi.org/10.4315/0362-028x-67.12.2839
Teunis, P. F. M., Sukhrie, F. H. A., Vennema, H., Bogerman, J., Beersma, M. F. C., & Koopmans, M. P. G. (2015). Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiology & Infection, 143(8), 1710–1717. https://doi.org/10.1017/S095026881400274X
Turner, E. R., Luo, Y., & Buchanan, R. L. (2020). Microgreen nutrition, food safety, and shelf life: A review. Journal of Food Science, 85(4), 870–882. https://doi.org/10.1111/1750-3841.15049
Urbanucci, A., Myrmel, M., Berg, I., von Bonsdorff, C.-H., & Maunula, L. (2009). Potential internalisation of caliciviruses in lettuce. International Journal of Food Microbiology, 135(2), 175–178. https://doi.org/10.1016/j.ijfoodmicro.2009.07.036
U.S. Food and Drug Administration. (2018). Greenbelt Greenhouse Ltd Recalls Greenbelt Microgreens Brand Microgreens Because of Possible Health Risk. U.S. Food and Drug Administration. FDA. https://www.fda.gov/safety/recalls-market-withdrawals-safety-alerts/greenbelt-greenhouse-ltd-recalls-greenbelt-microgreens-brand-microgreens-because-possible-health. Accessed 8 July 2021.
Vasickova, P., Pavlik, I., Verani, M., & Carducci, A. (2010). Issues Concerning Survival of Viruses on Surfaces. Food and Environmental Virology, 2(1), 24–34. https://doi.org/10.1007/s12560-010-9025-6
Verlinden, S. (2020). Microgreens. In Horticultural reviews (pp. 85–124). John Wiley & Sons, Ltd. https://doi.org/10.1002/9781119625407.ch3
Wang, Q., & Kniel, K. E. (2016). Survival and transfer of murine norovirus within a hydroponic system during kale and mustard microgreen harvesting. Applied and Environmental Microbiology, 82(2), 705–713. https://doi.org/10.1128/AEM.02990-15
Yépiz-Gómez, M. S., Gerba, C. P., & Bright, K. R. (2013). Survival of respiratory viruses on fresh produce. Food and Environmental Virology, 5(3), 150–156. https://doi.org/10.1007/s12560-013-9114-4
Zhang, X., He, J., Huang, W., Huang, H., Zhang, Z., Wang, J., et al. (2018). Antiviral Activity of the Sesquiterpene Lactones from Centipeda minima against Influenza a Virus in vitro. Natural Product Communications. https://doi.org/10.1177/1934578X1801300201
Zhang, X., Xia, Y., Yang, L., He, J., Li, Y., & Xia, C. (2019). Brevilin A, a sesquiterpene lactone, inhibits the replication of influenza a virus in vitro and in vivo. Viruses, 11(9), E835. https://doi.org/10.3390/v11090835
Acknowledgements
The authors thank Dr. Adam Baker for his assistance with ESEM as well as reviewing the manuscript. We also thank Dr. Stanley Flegler at Michigan State University for his guidance on the appropriate preparation of our samples for SEM imaging.
Funding
This research was supported by a University of Arkansas Graduate Professional Student Congress Research Council Research Grant received by Wenjun Deng. This work was also supported in part by the National Institute of Food and Agriculture (NIFA), U.S. Department of Agriculture (USDA), Hatch Act Funding.
Author information
Authors and Affiliations
Contributions
Conceptualization, WD and KEG; Methodology, WD and KEG; Formal Analysis, WD; Investigation, WD; Resources, KEG; Writing—Original Draft, WD; Writing—Reviewing and Editing, WD and KEG; Visualization, WD; Supervision, KEG; Funding Acquisition, KEG.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no financial or proprietary interests in any material discussed in this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Deng, W., Gibson, K.E. Microgreen Variety Impacts Leaf Surface Persistence of a Human Norovirus Surrogate. Food Environ Virol 15, 82–88 (2023). https://doi.org/10.1007/s12560-022-09536-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12560-022-09536-x