Abstract
Foodborne disease outbreaks linked to consumption of vegetables have been often attributed to human enteric viruses, such as Norovirus (NoV), Hepatitis A virus (HAV), and Rotavirus (RoV). Information about the occurrence of these viruses is scarce in many fresh-producing countries. Viral contamination detection of indicators, such as somatic coliphages, could indirectly reflect the presence of viral pathogens, being a valuable tool for better viral risk assessment in food industry. This study aimed to establish the occurrence and correlation of foodborne viruses and somatic coliphages in leafy greens in northern Mexico. A total of 320 vegetable samples were collected, resulting in 80 composite rinses, 40 of lettuce and 40 of parsley. Somatic coliphages were determined using the EPA 1602 method, while foodborne viruses (HAV, RoV, NoV GI, and GII) were determined by qPCR. The occurrence of RoV was 22.5% (9/40, mean 2.11 log gc/g) in lettuce and 20% (8/40, mean 1.91 log gc/g) in parsley. NoV and HAV were not detected in any samples. Somatic coliphages were present in all lettuce and parsley samples, with mean levels of 1.85 log PFU/100 ml and 2.28 log PFU/100 ml, respectively. Spearman analysis established the correlation of somatic coliphages and genomic copies of RoV, resulting in an r2 value of − 0.026 in lettuce and 0.349 in parsley. Although NoV or HAV were undetected in the samples, the presence of RoV is a matter of concern as leafy greens are usually eaten raw, which poses a potential risk of infection.
Similar content being viewed by others
References
Adefisoye, M. A., Nwodo, U. U., Green, E., & Okoh, A. I. (2016). Quantitative PCR detection and characterisation of human adenovirus, rotavirus and hepatitis A virus in discharged effluents of two wastewater treatment facilities in the Eastern Cape South Africa. Food and Environmental Virology, 8(4), 262–274. https://doi.org/10.1007/S12560-016-9246-4/FIGURES/3
Apruzzese, I., Song, E., Bonah, E., Sanidad, V. S., Leekitcharoenphon, P., Medardus, J. J., Abdalla, N., Hosseini, H., & Takeuchi, M. (2019). Investing in food safety for developing countries: Opportunities and challenges in applying whole-genome sequencing for food safety management. Foodborne Pathogens and Disease, 16(7), 463–473. https://doi.org/10.1089/FPD.2018.2599
Atabakhsh, P., Kargar, M., & Doosti, A. (2021). Detection and evaluation of rotavirus surveillance methods as viral indicator in the aquatic environments. Brazilian Journal of Microbiology, 52(2), 811. https://doi.org/10.1007/S42770-020-00417-8
Bachofen, C. (2018). Selected viruses detected on and in our food. Current Clinical Microbiology Reports, 5(2), 143. https://doi.org/10.1007/S40588-018-0087-9
Baert, L., Uyttendaele, M., & Debevere, J. (2008). Evaluation of viral extraction methods on a broad range of Ready-To-Eat foods with conventional and real-time RT-PCR for Norovirus GII detection. International Journal of Food Microbiology, 123(1–2), 101–108. https://doi.org/10.1016/j.ijfoodmicro.2007.12.020
Ballesté, E., Blanch, A. R., Mendez, J., Sala-Comorera, L., Maunula, L., Monteiro, S., Farnleitner, A. H., Tiehm, A., Jofre, J., & García-Aljaro, C. (2021). Bacteriophages are good estimators of human viruses present in water. Frontiers in Microbiology. https://doi.org/10.3389/FMICB.2021.619495
Bartz, F. E., Hodge, D. W., Heredia, N., de Aceituno, A. F., Solís, L., Jaykus, L. A., Garcia, S., & Leon, J. S. (2016). Somatic coliphage profiles of produce and environmental samples from farms in northern México. Food and Environmental Virology, 8(3), 221–226. https://doi.org/10.1007/s12560-016-9240-x
Bartz, F. E., Lickness, J. S., Heredia, N., de Aceituno, A. F., Newman, K. L., Hodge, D. W., Jaykus, L. A., García, S., & Leon, J. S. (2017). Contamination of fresh produce by microbial indicators on farms and in packing facilities: Elucidation of environmental routes. Applied and Environmental Microbiology, 83, e02984–16.
Bennett, S. D., Sodha, S. V., Ayers, T. L., Lynch, M. F., Gould, L. H., & Tauxe, R. V. (2018). Produce-associated foodborne disease outbreaks, USA, 1998–2013. Epidemiology and Infection, 146(11), 1397–1406. https://doi.org/10.1017/S0950268818001620
Bosch, A., Gkogka, E., Le Guyader, F. S., Loisy-Hamon, F., Lee, A., van Lieshout, L., Marthi, B., Myrmel, M., Sansom, A., Schultz, A. C., Winkler, A., Zuber, S., & Phister, T. (2018). Foodborne viruses: Detection, risk assessment, and control options in food processing. In International Journal of Food Microbiology (Vol. 285, pp. 110–128). Elsevier B.V. https://doi.org/10.1016/j.ijfoodmicro.2018.06.001
Chacón, L., Barrantes, K., Santamaría-Ulloa, C., Solano, M., Reyes, L., Taylor, L., Valiente, C., Symonds, E. M., & Achí, R. (2020). A somatic coliphage threshold approach to improve the management of activated sludge wastewater treatment plant effluents in resource-limited regions. Applied and Environmental Microbiology. https://doi.org/10.1128/AEM.00616
Chan, P. K. S., Guan, H., & Chan, M. C. W. (2017). The norovirus: Features, detection and prevention of foodborne disease. Academic Press.
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
Chin, N. A., Salihah, N. T., Shivanand, P., & Ahmed, M. U. (2022). Recent trends and developments of PCR-based methods for the detection of food-borne Salmonella bacteria and Norovirus. Journal of Food Science and Technology, 59(12), 4570–4582. https://doi.org/10.1007/S13197-021-05280-5
Cho, K., Lee, C., Park, S. J., Kim, J. H., Choi, Y. S., Kim, M. S., Koo, E. S., Yoon, H. J., Kang, J. H., Jeong, Y. S., Choi, J. D., & Ko, G. P. (2018). Use of coliphages to investigate norovirus contamination in a shellfish growing area in Republic of Korea. Environmental Science and Pollution Research, 25(30), 30044–30055. https://doi.org/10.1007/s11356-018-2857-6
Church, J. A., Rukobo, S., Govha, M., Lee, B., Carmolli, M. P., Chasekwa, B., Ntozini, R., Mutasa, K., McNeal, M. M., Majo, F. D., Tavengwa, N. V., Moulton, L. H., Humphrey, J. H., Kirkpatrick, B. D., & Prendergast, A. J. (2019). The impact of improved water, sanitation, and hygiene on oral rotavirus vaccine immunogenicity in Zimbabwean infants: Substudy of a cluster-randomized trial. Clinical Infectious Diseases, 69(12), 2074. https://doi.org/10.1093/CID/CIZ140
Coudray-Meunier, C., Fraisse, A., Martin-Latil, S., Guillier, L., Delannoy, S., Fach, P., & Perelle, S. (2015). A comparative study of digital RT-PCR and RT-qPCR for quantification of hepatitis A virus and norovirus in lettuce and water samples. International Journal of Food Microbiology, 201, 17–26. https://doi.org/10.1016/j.ijfoodmicro.2015.02.006
Crawford, S. E., Ramani, S., Tate, J. E., Parashar, U. D., Svensson, L., Hagbom, M., Franco, M. A., Greenberg, H. B., O’Ryan, M., Kang, G., Desselberger, U., & Estes, M. K. (2017). Rotavirus infection. Nature Reviews Disease Primers. https://doi.org/10.1038/nrdp.2017.83
Cuevas-Ferrando, E., Pérez-Cataluña, A., Falcó, I., Randazzo, W., & Sánchez, G. (2022). Monitoring human viral pathogens reveals potential hazard for treated wastewater discharge or reuse. Frontiers in Microbiology, 13, 836193. https://doi.org/10.3389/FMICB.2022.836193/BIBTEX
de Castro Carvalho, S. V., Rogovski, P., Cadamuro, R. D., Viancelli, A., Michelon, W., Dos Reis, D. A., Santana Chagas, I. A., Assenço, R., da Silva Lanna, M. C., Treichel, H., & Fongaro, G. (2020). Co-contamination of food products from family farms in an environmental disaster area in Southeast Brazil with pathogenic bacteria and enteric viruses. Archives of Virology, 165(3), 715–718. https://doi.org/10.1007/s00705-019-04501-9
DePaola, A., Jones, J. L., Woods, J., Burkhardt, W., Calci, K. R., Krantz, J. A., Bowers, J. C., Kasturi, K., Byars, R. H., Jacobs, E., Williams-Hill, D., Nabe, K., & Nabe, K. (2010). Bacterial and viral pathogens in live oysters: 2007 United States market survey. Applied and Environmental Microbiology, 76(9), 2754–2768. https://doi.org/10.1128/AEM.02590-09
Dewey-Mattia, D., Manikonda, K., Hall, A. J., Wise, M. E., & Crowe, S. J. (2019). Surveillance for foodborne disease outbreaks—United States, 2009–2015 MMWR. Surveillance Summaries, 67(10), 1–11. https://doi.org/10.15585/MMWR.SS6710A1
Donaldson, A. L., Harris, J. P., Vivancos, R., & O’Brien, S. J. (2022). Can cases and outbreaks of norovirus in children provide an early warning of seasonal norovirus infection: An analysis of nine seasons of surveillance data in England UK. BMC Public Health, 22(1), 1–10. https://doi.org/10.1186/S12889-022-13771-Z/TABLES/5
Ekundayo, T. C., & Ijabadeniyi, O. A. (2023). Human norovirus contamination challenge in fresh produce: a global prevalence and meta-analytic assessment. Journal of Applied Microbiology. https://doi.org/10.1093/JAMBIO/LXAC009
Elmahdy, E. M., Shaheen, M. N. F., Mahmoud, L. H. I., Hammad, I. A., & Soliman, E. R. S. (2022). Detection of norovirus and hepatitis A virus in strawberry and green leafy vegetables by using RT-qPCR in Egypt. Food and Environmental Virology, 14(2), 178–189. https://doi.org/10.1007/S12560-022-09516-1/METRICS
Ferguson, A. S., Layton, A. C., Mailloux, B. J., Culligan, P. J., Williams, D. E., Smartt, A. E., Sayler, G. S., Feighery, J., McKay, L. D., Knappett, P. S. K., Alexandrova, E., Arbit, T., Emch, M., Escamilla, V., Ahmed, K. M., Alam, M. J., Streatfield, P. K., Yunus, M., & van Geen, A. (2012). Comparison of fecal indicators with pathogenic bacteria and rotavirus in groundwater. Science of the Total Environment, 431, 314–322. https://doi.org/10.1016/j.scitotenv.2012.05.060
Formiga-Cruz, M., Allard, A. K., Conden-Hansson, A. C., Henshilwood, K., Hernroth, B. E., Jofre, J., Lees, D. N., Lucena, F., Papapetropoulou, M., Rangdale, R. E., Tsibouxi, A., Vantarakis, A., & Girones, R. (2003). Evaluation of potential indicators of viral contamination in shellfish and their applicability to diverse geographical areas. Applied and Environmental Microbiology, 69(3), 1556–1563. https://doi.org/10.1128/AEM.69.3.1556-1563.2003
Fout, G. S., Cashdollar, J. L., Griffin, S. M., Brinkman, N. E., Varughese, E. A., & Parshionikar, S. U. (2016). EPA method 1615. Measurement of enterovirus and norovirus occurrence in water by culture and RT-qPCR. Part III. Virus detection by RT-qPCR. Journal of Visualized Experiments: Jove, 107, e52646. https://doi.org/10.3791/52646
Heredia, N., Caballero, C., Cárdenas, C., Molina, K., García, R., Solís, L., Burrowes, V., Bartz, F. E., Fabiszewski De Aceituno, A., Jaykus, L. A., García, S., & Leon, J. (2016). Microbial indicator profiling of fresh produce and environmental samples from farms and packing facilities in northern Mexico. Journal of Food Protection, 79, 1197–1209.
Hida, K., Papafragkou, E., & Kulka, M. (2018). Testing for human norovirus and recovery of process control in outbreak-associated produce items. Journal of Food Protection, 81(1), 105–114. https://doi.org/10.4315/0362-028X.JFP-17-134
Hot, D., Legeay, O., Jacques, J., Gantzer, C., Caudrelier, Y., Guyard, K., Lange, M., & Andréoletti, L. (2003). Detection of somatic phages, infectious enteroviruses and enterovirus genomes as indicators of human enteric viral pollution in surface water. Water Research, 37(19), 4703–4710. https://doi.org/10.1016/S0043-1354(03)00439-1
ISO 15216-1:2017—Microbiology of the food chain—Horizontal method for determination of hepatitis A virus and norovirus using real-time RT-PCR—Part 1: Method for quantification. (2017). Retrieved from https://www.iso.org/standard/65681.html
Ito, E., Pu, J., Miura, T., Kazama, S., Nishiyama, M., Ito, H., Konta, Y., Omura, T., & Watanabe, T. (2021). Detection of Rotavirus vaccine strains in Oysters and Sewage and their relationship with the gastroenteritis epidemic. Applied and Environmental Microbiology, 87(10), 1–9. https://doi.org/10.1128/AEM.02547-20
Kittigul, L., Panjangampatthana, A., Rupprom, K., & Pombubpa, K. (2014). Genetic diversity of Rotavirus strains circulating in environmental water and Bivalve Shellfish in Thailand. International Journal of Environmental Research and Public Health, 11(2), 1299–1311. https://doi.org/10.3390/IJERPH110201299
Kraay, A. N. M., Brouwer, A. F., Lin, N., Collender, P. A., Remais, J. V., & Eisenberg, J. N. S. (2018). Modeling environmentally mediated rotavirus transmission: The role of temperature and hydrologic factors. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/PNAS.1719579115/-/DCSUPPLEMENTAL
León-Félix, J., Martínez-Bustillos, R. A., Báez-Sañudo, M., Peraza-Garay, F., & Chaidez, C. (2010). Norovirus contamination of bell pepper from handling during harvesting and packing. Food and Environmental Virology, 4(2), 211–217. https://doi.org/10.1007/S12560-010-9048-Z
Li, D., De Keuckelaere, A., & Uyttendaele, M. (2015). Fate of foodborne viruses in the “Farm to Fork” chain of fresh produce. Comprehensive Reviews in Food Science and Food Safety, 14(6), 755. https://doi.org/10.1111/1541-4337.12163
Liang, L., Goh, S. G., Vergara, G. G. R. V., Fang, H. M., Rezaeinejad, S., Chang, S. Y., Bayen, S., Lee, W. A., Sobsey, M. D., Rose, J. B., & Gin, K. Y. H. (2015). Alternative fecal indicators and their empirical relationships with enteric viruses, Salmonella enterica, and Pseudomonas aeruginosa in surface waters of a tropical urban catchment. Applied and Environmental Microbiology, 81(3), 850–860. https://doi.org/10.1128/AEM.02670-14
Logan, C., O’Leary, J. J., & O’Sullivan, N. (2006). Real-time reverse transcription-PCR for detection of rotavirus and adenovirus as causative agents of acute viral gastroenteritis in children. Journal of Clinical Microbiology, 44(9), 3189–3195. https://doi.org/10.1128/JCM.00915-06
Lowther, J. A., Bosch, A., Butot, S., Ollivier, J., Mäde, D., Rutjes, S. A., Hardouin, G., Lombard, B., In’t Veld, P., & Leclercq, A. (2019). Validation of EN ISO method 15216—Part 1—Quantification of hepatitis A virus and norovirus in food matrices. International Journal of Food Microbiology, 288, 82–90. https://doi.org/10.1016/J.IJFOODMICRO.2017.11.014
Melgaço, F. G., Corrêa, A. A., Ganime, A. C., Brandão, M. L., Medeiros, V. D., Rosas, C. D., Lopes, S. M., & Miagostovich, M. P. (2018). Evaluation of skimmed milk flocculation method for virus recovery from tomatoes. Brazilian Journal of Microbiology, 49, 34–39. https://doi.org/10.1016/j.bjm.2018.04.014
Nappier, S. P., Hong, T., Ichida, A., Goldstone, A., & Eftim, S. E. (2019). Occurrence of coliphage in raw wastewater and in ambient water: A meta-analysis. Water Research, 153, 263–273. https://doi.org/10.1016/J.WATRES.2018.12.058
National Outbreak Reporting System (NORS) Dashboard|CDC. (n.d.). Retrieved June 15, 2023, from https://wwwn.cdc.gov/norsdashboard/
Nasheri, N., Vester, A., & Petronella, N. (2019). Foodborne viral outbreaks associated with frozen produce. Epidemiology and Infection, 147, e291. https://doi.org/10.1017/S0950268819001791
Ngazoa, E. S., Fliss, I., & Jean, J. (2008). Quantitative study of persistence of human norovirus genome in water using TaqMan real-time RT-PCR. Journal of Applied Microbiology, 104(3), 707–715. https://doi.org/10.1111/j.1365-2672.2007.03597.x
Pan, L., Zhang, Q., Li, X., & Tian, P. (2012). Detection of human norovirus in cherry tomatoes, blueberries and vegetable salad by using a receptor-binding capture and magnetic sequestration (RBCMS) method. Food Microbiology, 30(2), 420–426. https://doi.org/10.1016/j.fm.2011.12.026
Pearce-Walker, J., Bright, K. R., Canales, R. A., Wilson, A. M., & Verhougstraete, M. P. (2020). Managing leafy green safety from adenoviruses and enteroviruses in irrigation water. Agricultural Water Management, 240, 106272. https://doi.org/10.1016/J.AGWAT.2020.106272
Pexara, A., & Govaris, A. (2020). Foodborne viruses and innovative non-thermal food-processing technologies. Foods. https://doi.org/10.3390/FOODS9111520
Richards, G. P., Watson, M. A., Meade, G. K., Hovan, G. L., & Kingsley, D. H. (2012). Resilience of norovirus GII.4 to freezing and thawing: Implications for virus infectivity. Food and Environmental Virology, 4(4), 192–197. https://doi.org/10.1007/s12560-012-9089-6
Richardson, V., Hernandez-Pichardo, J., Quintanar-Solares, M., Esparza-Aguilar, M., Johnson, B., Gomez-Altamirano, C. M., Parashar, U., & Patel, M. (2010). Effect of rotavirus vaccination on death from childhood diarrhea in Mexico. The New England Journal of Medicine, 362(4), 299–305. https://doi.org/10.1056/NEJMOA0905211
Rohr, J. R., Barrett, C. B., Civitello, D. J., Craft, M. E., Delius, B., DeLeo, G. A., Hudson, P. J., Jouanard, N., Nguyen, K. H., Ostfeld, R. S., Remais, J. V., Riveau, G., Sokolow, S. H., & Tilman, D. (2019). Emerging human infectious diseases and the links to global food production. Nature Sustainability, 2(6), 445–456. https://doi.org/10.1038/s41893-019-0293-3
Salvo, M., Azambuya, J., Baccardatz, N., Moriondo, A., Blanco, R., Martinez, M., Direnna, M., Bertolini, G., Gamazo, P., Colina, R., Alvareda, E., & Victoria, M. (2022). One-year surveillance of SARS-CoV-2 and Rotavirus in water matrices from a hot spring area. Food and Environmental Virology, 14(4), 401–409. https://doi.org/10.1007/S12560-022-09537-W/FIGURES/5
Savichtcheva, O., & Okabe, S. (2006). Alternative indicators of fecal pollution: Relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. In Water Research (Vol. 40, Issue 13, pp. 2463–2476). Elsevier Ltd. https://doi.org/10.1016/j.watres.2006.04.040
Severi, E., Vennema, H., Takkinen, J., Lopalco, P. L., & Coulombier, D. (2015). Hepatitis A outbreaks. The Lancet Infectious Diseases, 15(6), 632–634. https://doi.org/10.1016/S1473-3099(15)00021-3
Shukla, S., Cho, H., Kwon, O. J., Chung, S. H., & Kim, M. (2018). Prevalence and evaluation strategies for viral contamination in food products: Risk to human health-a review. Critical Reviews in Food Science and Nutrition, 58(3), 405–419. https://doi.org/10.1080/10408398.2016.1182891
Singh, S., Pitchers, R., & Hassard, F. (2022). Coliphages as viral indicators of sanitary significance for drinking water. Frontiers in Microbiology. https://doi.org/10.3389/FMICB.2022.941532
Sobolik, J. S., Newman, K. L., Jaykus, L. A., Bihn, E. A., & Leon, J. S. (2021). Norovirus transmission mitigation strategies during simulated produce harvest and packing. International Journal of Food Microbiology. https://doi.org/10.1016/J.IJFOODMICRO.2021.109365
Stals, A., Baert, L., Jasson, V., Van Coillie, E., & Uyttendaele, M. (2011). Screening of fruit products for norovirus and the difficulty of interpreting positive PCR results. Journal of Food Protection, 74(3), 425–431. https://doi.org/10.4315/0362-028X.JFP-10-209
Torok, V. A., Hodgson, K. R., Jolley, J., Turnbull, A., & McLeod, C. (2019). Estimating risk associated with human norovirus and hepatitis A virus in fresh Australian leafy greens and berries at retail. International Journal of Food Microbiology. https://doi.org/10.1016/j.ijfoodmicro.2019.108327
United States Environmental Protection Agency. (2001). US EPA Method 1602: Male-specific (F+) and Somatic Coliphage in Water by Single Agar Layer (SAL) Procedure.
Van Zyl, W. B., Page, N. A., Grabow, W. O. K., Steele, A. D., & Taylor, M. B. (2006). Molecular epidemiology of group A rotaviruses in water sources and selected raw vegetables in Southern Africa. Applied and Environmental Microbiology, 72(7), 4554. https://doi.org/10.1128/AEM.02119-05
Victor, C. P., Ellis, K., Lamar, F., & Leon, J. S. (2021). Agricultural detection of norovirus and hepatitis A using fecal indicators: A systematic review. International Journal of Microbiology. https://doi.org/10.1155/2021/6631920
Vital, P. G., Dimasuay, K. G. B., Widmer, K. W., & Rivera, W. L. (2014). Microbiological quality of fresh produce from open air markets and supermarkets in the Philippines. The Scientific World Journal. https://doi.org/10.1155/2014/219534
Wu, J., Long, S. C., Das, D., & Dorner, S. M. (2011). Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. Journal of Water and Health, 9(2), 265–278. https://doi.org/10.2166/wh.2011.117
Acknowledgements
Authors express their gratitude to the Mexican Consejo Nacional de Ciencia y Tecnología (CONACYT) for the scholarships granted to Fernanda Flores-Rodríguez and Axel Ossio.
Funding
There were no institutions funding this research.
Author information
Authors and Affiliations
Contributions
Conceptualization: JAM-M, NH, SG; Investigation: AO, FF-R; Formal Analysis: AO; Project Administration: JAM-M; Supervision: NH, SG; Writing—original draft: AO, JAM-M, Writing—review & editing: NH, SG, JAM-M; Resources: SG, NH; Validation: JAM-M; Visualization: AO; Methodology: AO.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ossio, A., Flores-Rodríguez, F., Heredia, N. et al. Foodborne Viruses and Somatic Coliphages Occurrence in Fresh Produce at Retail from Northern Mexico. Food Environ Virol 16, 109–119 (2024). https://doi.org/10.1007/s12560-023-09578-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12560-023-09578-9