Abstract
Human noroviruses (HuNoVs) can be easily transferred by the contacts of humans or fomites. Swab sampling methods are widely used for recovering HuNoVs from small surfaces of various fomites or hard-to-reach locations and swab sampling conditions are important for the accurate detection of HuNoVs, which have a low infectious dose and relatively long persistence under a range of environmental conditions. Therefore, to determine the suitable swab sampling method for recovering HuNoVs from various surfaces, we evaluated combinations of four swab materials (cotton, microdenier polyester [a type of microfiber], polyurethane foam, and rayon) and three elution buffer solutions (phosphate-buffered saline [PBS], PBS with 0.2% Tween-80, and 3% beef extract-50 mM glycine [pH 9.5]). First, we inoculated HuNoVs or murine noroviruses (MuNoVs), the surrogate of HuNoVs, onto test coupons (10 × 10 cm) consisting of three common surface materials (high-density polyethylene, stainless steel, and wood). Coupons were swabbed using a combination of each swab material and elution buffer, and the viral recovery was measured by real-time reverse transcription quantitative polymerase chain reaction (RT-qPCR) or plaque assay. By RT-qPCR, we confirmed that the cotton swab–PBS and microdenier polyester–PBS combinations had recovery efficiencies greater than 80% for viruses on plastic and stainless steel surfaces. The cotton swab–PBS combination had the highest recovery efficiency on all surface materials via the plaque assay. Therefore, a cotton or a microdenier polyester swab with PBS could be a useful method for sampling HuNoVs on various surfaces.
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References
Ahmed, S. M., Hall, A. J., Robinson, A. E., Verhoef, L., Premkumar, P., Parashar, U. D., et al. (2014). Global prevalence of norovirus in cases of gastroenteritis: A systematic review and meta-analysis. The Lancet Infectious Diseases, 14(8), 725–730.
Barker, J., Vipond, I., & Bloomfield, S. (2004). Effects of cleaning and disinfection in reducing the spread of Norovirus contamination via environmental surfaces. Journal of Hospital Infection, 58(1), 42–49.
Boxman, I. L., Dijkman, R., te Loeke, N. A., Hägele, G., Tilburg, J. J., Vennema, H., et al. (2009). Environmental swabs as a tool in norovirus outbreak investigation, including outbreaks on cruise ships. Journal of Food Protection, 72(1), 111–119.
Cannon, J. L., Papafragkou, E., Park, G. W., Osborne, J., Jaykus, L.-A., & Vinjé, J. (2006). Surrogates for the study of norovirus stability and inactivation in the environment: A comparison of murine norovirus and feline calicivirus. Journal of Food Protection, 69(11), 2761–2765.
Centers for Disease Control and Prevention. (2012). Emergency response resources: surface sampling procedures for Bacillus anthracis spores from smooth, non-porous surfaces. https://www.cdc.gov/niosh/topics/emres/surface-sampling-bacillus-anthracis.html. Accessed 26 July 2018.
Cheesbrough, J. S., Green, J., Gallimore, C. I., Wright, P. A., & Brown, D. W. (2000). Widespread environmental contamination with Norwalk-like viruses (NLV) detected in a prolonged hotel outbreak of gastroenteritis. Epidemiology and Infection, 125(1), 93–98.
D’Souza, D. H., Sair, A., Williams, K., Papafragkou, E., Jean, J., Moore, C., et al. (2006). Persistence of caliciviruses on environmental surfaces and their transfer to food. International Journal of Food Microbiology, 108(1), 84–91.
De Keuckelaere, A., Stals, A., & Uyttendaele, M. (2014). Semi-direct lysis of swabs and evaluation of their efficiencies to recover human noroviruses GI and GII from surfaces. Food and Environmental Virology, 6(2), 132–139.
Deng, S., & Bai, R. B. (2003). Aminated polyacrylonitrile fibers for humic acid adsorption: Behaviors and mechanisms. Environmental Science and Technology, 37(24), 5799–5805.
Ganime, A. C., Leite, J. P. G., de Abreu Corrêa, A., Melgaço, F. G., Carvalho-Costa, F. A., & Miagostovich, M. P. (2015). Evaluation of the swab sampling method to recover viruses from fomites. Journal of Virological Methods, 217, 24–27.
Giammanco, G. M., Di Bartolo, I., Purpari, G., Costantino, C., Rotolo, V., Spoto, V., et al. (2014). Investigation and control of a Norovirus outbreak of probable waterborne transmission through a municipal groundwater system. Journal of Water and Health, 12(3), 452–464.
Gilbert, S. E., Rose, L. J., Howard, M., Bradley, M. D., Shah, S., Silvestri, E., et al. (2014). Evaluation of swabs and transport media for the recovery of Yersinia pestis. Journal of Microbiological Methods, 96, 35–41.
Ibfelt, T., Frandsen, T., Permin, A., Andersen, L. P., & Schultz, A. C. (2016). Test and validation of methods to sample and detect human virus from environmental surfaces using norovirus as a model virus. Journal of Hospital Infection, 92(4), 378–384.
Jiang, X., Wang, M., Wang, K., & Estes, M. K. (1993). Sequence and genomic organization of Norwalk virus. Virology, 195(1), 51–61.
Jones, E. L., Kramer, A., Gaither, M., & Gerba, C. P. (2007). Role of fomite contamination during an outbreak of norovirus on houseboats. International Journal of Environmental Health Research, 17(2), 123–131.
Julian, T. R., Tamayo, F. J., Leckie, J. O., & Boehm, A. B. (2011). Comparison of surface sampling methods for virus recovery from fomites. Applied and Environmental Microbiology, 77(19), 6918–6925.
Kapikian, A. Z., Wyatt, R. G., Dolin, R., Thornhill, T. S., Kalica, A. R., & Chanock, R. M. (1972). Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. Journal of Virology, 10(5), 1075–1081.
Kephart, C. M., & Bushon, R. N. (2010). Utility of microbial source-tracking markers for assessing fecal contamination in the Portage River watershed, northwestern Ohio, 2008. US Geological Survey. https://pubs.usgs.gov/sir/2010/5036/. Accessed 17 April 2018.
Lamhoujeb, S., Fliss, I., Ngazoa, S. E., & Jean, J. (2008). Evaluation of the persistence of infectious human noroviruses on food surfaces by using real-time nucleic acid sequence-based amplification. Applied and Environmental Microbiology, 74(11), 3349–3355.
Lee, J., Zoh, K., & Ko, G. (2008). Inactivation and UV disinfection of murine norovirus with TiO2 under various environmental conditions. Applied and Environmental Microbiology, 74(7), 2111–2117.
Lowther, J. A., Bosch, A., Butot, S., Ollivier, J., Mäde, D., Rutjes, S. A., et al. (2017). Validation of ISO method 15216 part 1–Quantification of hepatitis A virus and norovirus in food matrices. International Journal of Food Microbiology. https://doi.org/10.1016/j.ijfoodmicro.2017.11.014.
Ministry of Food and Drug Safety. (2013). Guideline for investigation on the cause of food poisoning. Chapter 5. Ministry of Food and Drug Safety, Chungcheonbuk-do, Republic of Korea. (Korean).
Nenonen, N. P., Hannoun, C., Svensson, L., Torén, K., Andersson, L.-M., Westin, J., et al. (2014). Norovirus GII. 4 detection in environmental samples from patient rooms during nosocomial outbreaks. Journal of Clinical Microbiology, 52(7), 2352–2358.
Otter, J. A., Yezli, S., & French, G. L. (2011). The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infection Control and Hospital Epidemiology, 32(7), 687–699.
Park, G. W., Chhabra, P., & Vinjé, J. (2017). Swab sampling method for the detection of human norovirus on surfaces. Journal of Visualized Experiments, 120, e55205.
Park, G. W., Lee, D., Treffiletti, A., Hrsak, M., Shugart, J., & Vinjé, J. (2015). Evaluation of a new environmental sampling protocol for detection of human norovirus on inanimate surfaces. Applied and Environmental Microbiology, 81(17), 5987–5992.
Park, Y., Cho, Y.-H., Jee, Y., & Ko, G. (2008). Immunomagnetic separation combined with real-time reverse transcriptase PCR assays for detection of norovirus in contaminated food. Applied and Environmental Microbiology, 74(13), 4226–4230.
Patel, M. M., Hall, A. J., Vinjé, J., & Parashar, U. D. (2009). Noroviruses: A comprehensive review. Journal of Clinical Virology, 44(1), 1–8.
Piedrahita, C. T., Cadnum, J. L., Jencson, A. L., Shaikh, A. A., Ghannoum, M. A., & Donskey, C. J. (2017). Environmental surfaces in healthcare facilities are a potential source for transmission of Candida auris and other Candida species. Infection Control and Hospital Epidemiology, 38(9), 1107–1109.
Rönnqvist, M., Rättö, M., Tuominen, P., Salo, S., & Maunula, L. (2013). Swabs as a tool for monitoring the presence of norovirus on environmental surfaces in the food industry. Journal of Food Protection, 76(8), 1421–1428.
Rusin, P., Maxwell, S., & Gerba, C. (2002). Comparative surface-to-hand and fingertip-to-mouth transfer efficiency of gram-positive bacteria, gram-negative bacteria, and phage. Journal of Applied Microbiology, 93(4), 585–592.
Scherer, K., Mäde, D., Ellerbroek, L., Schulenburg, J., Johne, R., & Klein, G. (2009). Application of a swab sampling method for the detection of norovirus and rotavirus on artificially contaminated food and environmental surfaces. Food and Environmental Virology, 1(1), 42–49.
Teunis, P. F. M., Moe, C. L., Liu, P., Miller, S. E., Lindesmith, L., Baric, R. S., et al. (2008). Norwalk virus: How infectious is it? Journal of Medical Virology, 80(8), 1468–1476.
Turnage, N. L., & Gibson, K. E. (2017). Sampling methods for recovery of human enteric viruses from environmental surfaces. Journal of Virological Methods, 248, 31–38.
Vinjé, J. (2015). Advances in laboratory methods for detection and typing of norovirus. Journal of Clinical Microbiology, 53(2), 373–381.
Wadl, M., Scherer, K., Nielsen, S., Diedrich, S., Ellerbroek, L., Frank, C., et al. (2010). Food-borne norovirus-outbreak at a military base, Germany, 2009. BMC Infectious Diseases, 10(1), 30.
Wikswo, M. E., Kambhampati, A., Shioda, K., Walsh, K. A., Bowen, A., & Hall, A. J. (2015). Outbreaks of acute gastroenteritis transmitted by person-to-person contact, environmental contamination, and unknown modes of transmission—United States, 2009–2013. Morbidity and Mortality Weekly Report, 64(12), 1–16.
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This research was supported by a Grant (14162MFDS973) from Ministry of Food and Drug Safety in 2015 and the BK21 plus program of the National Research Foundation of Korea (NRF) (22A20130012682).
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Lee, C., Park, S., Cho, K. et al. Comparison of Swab Sampling Methods for Norovirus Recovery on Surfaces. Food Environ Virol 10, 378–385 (2018). https://doi.org/10.1007/s12560-018-9353-5
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DOI: https://doi.org/10.1007/s12560-018-9353-5