PMAxx-RT-qPCR to Determine Human Norovirus Inactivation Following High-Pressure Processing of Oysters.

التفاصيل البيبلوغرافية
العنوان:	PMAxx-RT-qPCR to Determine Human Norovirus Inactivation Following High-Pressure Processing of Oysters.
المؤلفون:	Rachmadi AT; Institute of Environmental Science and Research Ltd (ESR), Kenepuru Science Centre, PO Box 50348, Porirua, 5240, New Zealand., Gyawali P; Institute of Environmental Science and Research Ltd (ESR), Kenepuru Science Centre, PO Box 50348, Porirua, 5240, New Zealand., Summers G; The New Zealand Institute for Plant and Food Research Ltd (PFR), Private Bag 92169, Auckland, 1142, New Zealand., Jabed A; Institute of Environmental Science and Research Ltd (ESR), Kenepuru Science Centre, PO Box 50348, Porirua, 5240, New Zealand., Fletcher GC; The New Zealand Institute for Plant and Food Research Ltd (PFR), Private Bag 92169, Auckland, 1142, New Zealand., Hewitt J; Institute of Environmental Science and Research Ltd (ESR), Kenepuru Science Centre, PO Box 50348, Porirua, 5240, New Zealand. joanne.hewitt@esr.cri.nz.
المصدر:	Food and environmental virology [Food Environ Virol] 2024 Jun; Vol. 16 (2), pp. 171-179. Date of Electronic Publication: 2024 Mar 08.
نوع المنشور:	Journal Article; Evaluation Study
اللغة:	English
بيانات الدورية:	Publisher: Springer Country of Publication: United States NLM ID: 101483831 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1867-0342 (Electronic) Linking ISSN: 18670334 NLM ISO Abbreviation: Food Environ Virol Subsets: MEDLINE
أسماء مطبوعة:	Original Publication: New York : Springer
مواضيع طبية MeSH:	Norovirus/genetics , Norovirus/isolation & purification , Norovirus/physiology , Norovirus/classification , Norovirus/growth & development , Ostreidae/virology , Shellfish/virology , Virus Inactivation , Food Handling/methods , Real-Time Polymerase Chain Reaction/methods, Animals ; Humans ; Food Contamination/analysis ; Hydrostatic Pressure ; Propidium/chemistry ; Propidium/analogs & derivatives ; Azides/chemistry ; Caliciviridae Infections/virology
مستخلص:	Norovirus is the leading cause of viral gastroenteritis globally. While person-to-person transmission is most commonly reported route of infection, human norovirus is frequently associated with foodborne transmission, including through consumption of contaminated bivalve molluscan shellfish. Reverse transcription (RT)-qPCR is most commonly used method for detecting human norovirus detection in foods, but does not inform on its infectivity, posing challenges for assessing intervention strategies aimed at risk elimination. In this study, RT-qPCR was used in conjunction with a derivative of the photoreactive DNA binding dye propidium monoazide (PMAxx™) (PMAxx-RT-qPCR) to evaluate the viral capsid integrity of norovirus genogroup I and II (GI and GII) in shellfish following high pressure processing (HPP). Norovirus GI.3 and GII.4 bioaccumulated oysters were subjected to HPP at pressures of 300 and 450 MPa at 15 °C, and 300, 450 and 600 MPa at 20 °C. Samples were analysed using both RT-qPCR and PMAxx-RT-qPCR. For each sample, norovirus concentration (genome copies/g digestive tissue) determined by RT-qPCR was divided by the PMAxx-RT-qPCR concentration, giving the relative non-intact (RNI) ratio. The RNI ratio values relate to the amount of non-intact (non-infectious) viruses compared to fully intact (possible infectious) viruses. Our findings revealed an increasing RNI ratio value, indicating decreasing virus integrity, with increasing pressure and decreasing pressure. At 300 MPa, for norovirus GI, the median [95% confidence interval, CI] RNI ratio values were 2.6 [1.9, 3.0] at 15 °C compared to 1.1 [0.9, 1.8] at 20 °C. At 450 MPa, the RNI ratio values were 5.5 [2.9, 7.0] at 15 °C compared to 1.3 [1.0, 1.6] at 20 °C. At 600 MPa, the RNI ratio value was 5.1 [2.9, 13.4] at 20 °C. For norovirus GII, RT-qPCR and PMAxx-RT-qPCR detections were significantly reduced at 450 and 600 MPa at both 15 °C and 20 °C, with the median [95% CI] RNI ratio value at 300 MPa being 1.1 [0.8, 1.6]. Following HPP treatment, the use of PMAxx-RT-qPCR enables the selective detection of intact and potential infectious norovirus, enhancing our understanding of the inactivation profiles and supporting the development of more effective risk assessment strategies. (© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)
References:	Arcangeli, G., Terregino, C., De Benedictis, P., Zecchin, B., Manfrin, A., Rossetti, E., Magnabosco, C., Mancin, M., & Brutti, A. (2012). Effect of high hydrostatic pressure on murine norovirus in Manila clams. Letters in Applied Microbiology, 54(4), 325–329. https://doi.org/10.1111/j.1472-765X.2012.03211.x. (PMID: 10.1111/j.1472-765X.2012.03211.x22268557) Bányai, K., Estes, M. K., Martella, V., & Parashar, U. D. (2018). Viral gastroenteritis. Lancet, 392, 175–186. https://doi.org/10.1016/S0140-6736(18)31128-0. (PMID: 10.1016/S0140-6736(18)31128-0300258108883799) Campos, C., Goblick, J., Lee, R., Wittamore, K., & Lees, D. N. (2017). Determining the zone of impact of norovirus contamination in shellfish production areas through microbiological monitoring and hydrographic analysis. Water Research, 124, 556–565. https://doi.org/10.1016/j.watres.2017.08.021. (PMID: 10.1016/j.watres.2017.08.02128810227) Canh, V. D., Kasuga, I., Furumai, H., & Katayama, H. (2019). Viability RT-qPCR combined with sodium deoxycholate pre-treatment for selective quantification of infectious viruses in drinking water samples. Food and Environmental Virology, 11(1), 40–51. https://doi.org/10.1007/s12560-019-09368-2. (PMID: 10.1007/s12560-019-09368-230680674) de Graaf, M., Villabruna, N., & Koopmans, M. P. (2017). Capturing norovirus transmission. Current Opinion in Virology, 22, 64–70. https://doi.org/10.1016/j.coviro.2016.11.008. (PMID: 10.1016/j.coviro.2016.11.00828056379) Elizaquível, P., Aznar, R., & Sánchez, G. (2014). Recent developments in the use of viability dyes and quantitative PCR in the food microbiology field. Journal of Applied Microbiology, 116(1), 1–13. https://doi.org/10.1111/jam.12365. (PMID: 10.1111/jam.1236524119073) Estes, M. K., Ettayebi, K., Tenge, V. R., Murakami, K., Karandikar, U., Lin, S. C., Ayyar, B. V., Cortes-Penfield, N. W., Haga, K., Neill, F. H., Opekun, A. R., Broughman, J. R., Zeng, X. L., Blutt, S. E., Crawford, S. E., Ramani, S., Graham, D. Y., & Atmar, R. L. (2019). Human norovirus cultivation in nontransformed stem cell-derived human intestinal enteroid cultures: Success and challenges. Viruses, 11(7), 638. https://doi.org/10.3390/v11070638. (PMID: 10.3390/v11070638313367656669637) Ettayebi, K., Crawford, S. E., Murakami, K., Broughman, J. R., Karandikar, U., Tenge, V. R., Neill, F. H., Blutt, S. E., Zeng, X. L., Qu, L., Kou, B., Opekun, A. R., Burrin, D., Graham, D. Y., Ramani, S., Atmar, R. L., & Estes, M. K. (2016). Replication of human noroviruses in stem cell-derived human enteroids. Science, 353(6306), 1387–1393. https://doi.org/10.1126/science.aaf5211. (PMID: 10.1126/science.aaf5211275629565305121) Fittipaldi, M., Rodriguez, N. J., Codony, F., Adrados, B., Peñuela, G. A., & Morató, J. (2010). Discrimination of infectious bacteriophage T4 virus by propidium monoazide real-time PCR. Journal of Virological Methods, 168(1–2), 228–232. https://doi.org/10.1016/j.jviromet.2010.06.011. (PMID: 10.1016/j.jviromet.2010.06.01120599560) Govaris, A., & Pexara, A. (2021). Inactivation of foodborne viruses by high-pressure processing (HPP). Foods, 10(2), 215. https://doi.org/10.3390/foods10020215. (PMID: 10.3390/foods10020215334942247909798) Gyawali, P., Fletcher, G. C., McCoubrey, D.-J., & Hewitt, J. (2019). Norovirus in shellfish: An overview of post-harvest treatments and their challenges. Food Control, 99, 171–179. https://doi.org/10.1016/j.foodcont.2018.12.049. (PMID: 10.1016/j.foodcont.2018.12.049) Gyawali, P., & Hewitt, J. (2018). Detection of infectious noroviruses from wastewater and seawater using PEMAX™ treatment combined with RT-qPCR. Water, 10(7), 841. https://doi.org/10.3390/w10070841. (PMID: 10.3390/w10070841) Hardstaff, J. L., Clough, H. E., Lutje, V., McIntyre, K. M., Harris, J. P., Garner, P., & O’Brien, S. J. (2018). Foodborne and food-handler norovirus outbreaks: A systematic review. Foodborne Pathogens and Disease, 15(10), 589–597. https://doi.org/10.1089/fpd.2018.2452. (PMID: 10.1089/fpd.2018.2452301099586201779) Hewitt, J., Rivera-Aban, M., & Greening, G. E. (2009). Evaluation of murine norovirus as a surrogate for human norovirus and hepatitis A virus in heat inactivation studies. Journal of Applied Microbiology, 107(1), 65–71. (PMID: 10.1111/j.1365-2672.2009.04179.x192985117197740) Imamura, S., Kanezashi, H., Goshima, T., Suto, A., Ueki, Y., Sugawara, N., Ito, H., Zou, B., Uema, M., Noda, M., & Akimoto, K. (2017). Effect of high-pressure processing on human noroviruses in laboratory-contaminated oysters by bio-accumulation. Foodborne Pathogens and Disease, 14(9), 518–523. https://doi.org/10.1089/fpd.2017.2294. (PMID: 10.1089/fpd.2017.229428594572) ISO 15216-1:2017. (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. https://www.iso.org/standard/65681.html. Jeon, E. B., Choi, M., Kim, J. Y., Ha, K. S., Kwon, J. Y., Jeong, S. H., Lee, H., Jung, Y. J., Ha, J., & Park, S. (2020). Characterizing the effects of thermal treatment on human norovirus GII.4 viability using propidium monoazide combined with RT-qPCR and quality assessments in mussels. Food Control, 109, 106954. https://doi.org/10.1016/j.foodcont.2019.106954. (PMID: 10.1016/j.foodcont.2019.106954) Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., Takeda, N., & Katayama, K. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41(4), 1548–1557. https://doi.org/10.1128/JCM.41.4.1548-1557.2003. (PMID: 10.1128/JCM.41.4.1548-1557.200312682144153860) Karim, M. R., Fout, G. S., Johnson, C. H., White, K. M., & Parshionikar, S. U. (2015). Propidium monoazide reverse transcriptase PCR and RT-qPCR for detecting infectious enterovirus and norovirus. Journal of Virological Methods, 219, 51–61. https://doi.org/10.1016/j.jviromet.2015.02.020. (PMID: 10.1016/j.jviromet.2015.02.02025796356) Kazama, S., Miura, T., Masago, Y., Konta, K., Tohma, K., Manaka, T., Liu, X., Nakayama, T., Tanno, M., Saito, H., Oshitani, T., & Omura, T. (2017). Environmental surveillance of norovirus genogroups I and II for sensitive detection of epidemic variants. Applied and Environmental Microbiology, 83, e03406–e03416. https://doi.org/10.1128/AEM.03406-16. (PMID: 10.1128/AEM.03406-16282135465394333) Kingsley, D. H. (2014). High pressure processing of bivalve shellfish and HPP’s use as a virus intervention. Foods, 3(2), 336–350. https://doi.org/10.3390/foods3020336. (PMID: 10.3390/foods3020336282343235302369) Kingsley, D. H., Hoover, D. G., Papafragkou, E., & Richards, G. P. (2002). Inactivation of hepatitis A virus and a calicivirus by high hydrostatic pressure. Journal of Food Protection, 65(10), 1605–1609. https://doi.org/10.4315/0362-028x-65.10.1605. (PMID: 10.4315/0362-028x-65.10.160512380746) Langlet, J., Kaas, L., Croucher, D., & Hewitt, J. (2018). Effect of the shellfish proteinase K digestion method on norovirus capsid integrity. Food and Environmental Virology, 10, 151–158. https://doi.org/10.1007/s12560-018-9336-6. (PMID: 10.1007/s12560-018-9336-629417429) Leifels, M., Cheng, D., Sozzi, E., Shoults, D. C., Wuertz, S., Mongkolsuk, S., & Sirikanchana, K. (2020). Capsid integrity quantitative PCR to determine virus infectivity in environmental and food applications—a systematic review. Water Research X, 11, 100080. https://doi.org/10.1016/j.wroa.2020.100080. (PMID: 10.1016/j.wroa.2020.100080334909437811166) Leifels, M., Jurzik, L., Wilhelm, M., & Hamza, I. A. (2015). Use of ethidium monoazide and propidium monoazide to determine viral infectivity upon inactivation by heat, UV- exposure and chlorine. International Journal of Hygiene and Environmental Health, 218(8), 686–693. https://doi.org/10.1016/j.ijheh.2015.02.003. (PMID: 10.1016/j.ijheh.2015.02.00325747544) Leon, J. S., Kingsley, D. H., Montes, J. S., Richards, G. P., Lyon, G. M., Abdulhafid, G. M., Seitz, S. R., Fernandez, M. L., Teunis, P. F., Flick, G. J., & Moe, C. L. (2011). Randomized, double-blinded clinical trial for human norovirus inactivation in oysters by high hydrostatic pressure processing. Applied and Environmental Microbiology, 77(15), 5476–5482. https://doi.org/10.1128/AEM.02801-10. (PMID: 10.1128/AEM.02801-10217055523147477) Li, D., Tang, Q. J., Wang, J. F., Wang, Y. M., Zhao, Q., & Xue, C. H. (2009). Effects of high-pressure processing on murine norovirus-1 in oysters (Crassostrea gigas) in situ. Food Control, 20(11), 992–996. https://doi.org/10.1016/j.foodcont.2008.11.012. (PMID: 10.1016/j.foodcont.2008.11.012) Li, X., Chen, C., & Kingsley, D. (2013). The influence of temperature, pH, and water immersion on the high hydrostatic pressure inactivation of GI.1 and GII.4 human noroviruses. International Journal of Food Microbiology, 167(2), 138–143. https://doi.org/10.1016/j.ijfoodmicro.2013.08.020. (PMID: 10.1016/j.ijfoodmicro.2013.08.02024135670) Li, X., & Chen, H. (2015). Evaluation of the porcine gastric mucin binding assay for high-pressure-inactivation studies using murine norovirus and Tulane virus. Applied and Environmental Microbiology, 81(2), 515–521. https://doi.org/10.1128/AEM.02971-14. (PMID: 10.1128/AEM.02971-14253620634277584) Li, X., Huang, R., & Chen, H. (2017). Evaluation of assays to quantify infectious human norovirus for heat and high-pressure inactivation studies using Tulane virus. Food and Environmental Virology, 9(3), 314–325. https://doi.org/10.1007/s12560-017-9288-2. (PMID: 10.1007/s12560-017-9288-228238030) Lou, F., Neetoo, H., Chen, H., & Li, J. (2011). Inactivation of a human norovirus surrogate by high-pressure processing: Effectiveness, mechanism, and potential application in the fresh produce industry. Applied and Environmental Microbiology, 77(5), 1862–1871. https://doi.org/10.1128/AEM.01918-10. (PMID: 10.1128/AEM.01918-1021193662) Lou, F., Ye, M., Ma, Y., Li, X., DiCaprio, E., Chen, H., Krakowka, S., Hughes, J., Kingsley, D., & Li, J. (2015). A gnotobiotic pig model for determining human norovirus inactivation by high-pressure processing. Applied and Environmental Microbiology, 81(19), 6679–6687. https://doi.org/10.1128/AEM.01566-15. (PMID: 10.1128/AEM.01566-15261879684561694) Lowther, J. A., Gustar, N. E., Powell, A. L., Hartnell, R. E., & Lees, D. N. (2012). Two-year systematic study to assess norovirus contamination in oysters from commercial harvesting areas in the United Kingdom. Applied and Environmental Microbiology, 78(16), 5812–5817. https://doi.org/10.1128/AEM.01046-12. (PMID: 10.1128/AEM.01046-12226851513406157) Masago, Y., Konta, Y., Kaza, S., Inaba, M., Imagawa, T., Tohma, K., Saito, M., Suzuki, A., Oshitani, H., & Omura, T. (2016). Comparative evaluation of real-time PCR methods for human noroviruses in wastewater and human stool. PLoS ONE, 11, e0160825. https://doi.org/10.1371/journal.pone.0160825. (PMID: 10.1371/journal.pone.0160825275256544985124) Parshionikar, S., Laseke, I., & Fout, S. G. (2010). Use of propidium monoazide in reverse transcriptase PCR to distinguish between infectious and noninfectious enteric virus in water samples. Applied and Environmental Microbiology, 76(13), 4318–4326. (PMID: 10.1128/AEM.02800-09204727362897418) Rachmadi, A. T., Kitajima, M., Pepper, I. A., & Gerba, C. P. (2016). Enteric and indicator virus removal by surface flow wetlands. Science of the Total Environment, 542, 976–982. https://doi.org/10.1016/j.scitotenv.2015.11.001. (PMID: 10.1016/j.scitotenv.2015.11.00126562344) Randazzo, W., Khezri, M., Ollivier, J., Le Guyader, F. S., Rodríguez-Díaz, J., Aznar, R., & Sánchez, G. (2018). Optimization of PMAxx pretreatment to distinguish between human norovirus with intact and altered capsids in shellfish and sewage samples. International Journal of Food Microbiology, 266, 1–7. https://doi.org/10.1016/j.ijfoodmicro.2017.11.011. (PMID: 10.1016/j.ijfoodmicro.2017.11.01129156242) Randazzo, W., López-Gálvez, F., Allende, A., Aznar, R., & Sánchez, G. (2016). Evaluation of viability PCR performance for assessing norovirus infectivity in fresh-cut vegetables and irrigation water. International Journal of Food Microbiology, 229, 1–6. https://doi.org/10.1016/j.ijfoodmicro.2016.04.010. (PMID: 10.1016/j.ijfoodmicro.2016.04.01027085970) Richards, G. P. (2012). Critical review of norovirus surrogates in food safety research: Rationale for considering volunteer studies. Food and Environmental Virology, 4(1), 6–13. https://doi.org/10.1007/s12560-011-9072-7. (PMID: 10.1007/s12560-011-9072-722408689) Roy, P. K., Jeon, E. B., Kim, J. Y., & Park, S. Y. (2023). Application of high-pressure processing (or high hydrostatic pressure) for the inactivation of human norovirus in Korean traditionally preserved raw crab. Viruses, 15(7), 1599. https://doi.org/10.3390/v15071599. (PMID: 10.3390/v150715993751528510386741) Sánchez, G., Aznar, R., Martínez, A., & Rodrigo, D. (2011). Inactivation of human and murine norovirus by high-pressure processing. Foodborne Pathogens and Disease, 8(2), 249–253. https://doi.org/10.1089/fpd.2010.0667. (PMID: 10.1089/fpd.2010.066721034235) Sarmento, S. K., Guerra, C. R., Malta, F. C., Coutinho, R., Miagostovich, M. P., & Fumian, T. M. (2020). Human norovirus detection in bivalve shellfish in Brazil and evaluation of viral infectivity using PMA treatment. Marine Pollution Bulletin, 157, 111315. https://doi.org/10.1016/j.marpolbul.2020.111315. (PMID: 10.1016/j.marpolbul.2020.11131532658680) Takahashi, M., Okakura, Y., Takahashi, H., Yamane, H., Akashige, S., Kuda, T., & Kimura, B. (2019). Evaluation of inactivation of murine norovirus in inoculated shell oysters by high hydrostatic pressure treatment. Journal of Food Protection, 82(12), 2169–2173. https://doi.org/10.4315/0362-028X.JFP-19-186. (PMID: 10.4315/0362-028X.JFP-19-18631742443) Tong, L., Ding, G., Yang, M., Su, L., Wang, S., Wang, Y., Zheng, L., Zhou, D., & Zhao, F. (2023). High-hydrostatic-pressure inactivation of GI.5 and GII.4 human norovirus and effects on the physical, chemical, and taste characteristics of oyster (Crassostrea virginica). LWT Food Science and Technology. https://doi.org/10.1016/j.lwt.2023.114554. (PMID: 10.1016/j.lwt.2023.114554) Wales, S. Q., Pandiscia, A., Kulka, M., Sanchez, G., & Randazzo, W. (2024). Challenges for estimating human norovirus infectivity by viability RT-qPCR as compared to replication in human intestinal enteroids. International Journal of Food Microbiology, 411, 110507. https://doi.org/10.1016/j.ijfoodmicro.2023.110507. (PMID: 10.1016/j.ijfoodmicro.2023.11050738043474) Wolf, S., Hewitt, J., & Greening, G. E. (2010). Viral multiplex quantitative PCR assays for tracking sources of fecal contamination. Applied and Environmental Microbiology, 76(5), 1388–1394. https://doi.org/10.1128/AEM.02249-09. (PMID: 10.1128/AEM.02249-09200614552832383) Ye, M., Li, X., Kingsley, D. H., Jiang, X., & Chen, H. (2014). Inactivation of human norovirus in contaminated oysters and clams by high hydrostatic pressure. Applied and Environmental Microbiology, 80(7), 2248–2253. https://doi.org/10.1128/AEM.04260-13. (PMID: 10.1128/AEM.04260-13244875343993135)
معلومات مُعتمدة:	CAWX1801 Ministry of Business, Innovation and Employment
فهرسة مساهمة:	Keywords: High pressure processing; Norovirus inactivation; PMAxx; RT-qPCR; Shellfish safety
المشرفين على المادة:	36015-30-2 (Propidium) 0 (Azides) 0 (propidium monoazide)
تواريخ الأحداث:	Date Created: 20240308 Date Completed: 20240619 Latest Revision: 20240911
رمز التحديث:	20240911
DOI:	10.1007/s12560-024-09585-4
PMID:	38457095
قاعدة البيانات:	MEDLINE

Find this article in full text from Springer Verlag.

Full Text Finder

الوصف
تدمد:	1867-0342
DOI:	10.1007/s12560-024-09585-4