Shellfish: Risk for Norovirus Outbreaks and Sporadic Infections

Yıl 2018, , 340 - 350, 29.10.2018

Sevinç Sökel , Mehmet Kale , Sibel Hasırcıoğlu , Sibel Yavru Oğuz Gürsoy , Kübra Kocatürk

https://doi.org/10.24323/akademik-gida.475372

Cited By: 1

Öz

NoVs, previously known as Norwalk-like viruses from the Caliciviridae family, are non-enveloped,
positive-sense, single-stranded RNA viruses with icosahedral capsid symmetry.
NoV infection causes both secretory and osmotic diarrhea. A few NoV particles
are sufficient to produce infection. NoV is mainly spread by contaminated food
and water. Direct person-to-person contact or contact with contaminated
surfaces and fomites are also responsible for spreading the virus. In general,
epidemic and pandemic outbreaks occur due to NoVs. Sporadic cases have also
been reported. Outbreaks and sporadic infections have been reported to be
resulting from consumption of NoV contaminated shellfish (e.g. mussel, oyster,
and crab), soft red fruits (strawberry and raspberry), vegetables (lettuce,
tomatoes and parsley), bakery products, delicatessen meats, salads, sandwiches,
water and ice. NoV is responsible for more than half of nonbacterial diarrheal
diseases around the world. Outbreaks of NoV originating from shellfish such as
mussels and oysters are common in the world. It has been reported that
shellfish grown in virus contaminated waters and seafood products prepared for
consumption by infected individuals may play a role for outbreaks. Bivalve
molluscan shellfish, such as mussels and oysters, can filter out large
quantities of water as part of their feeding activities and, accumulate and concentrate viruses from
shallow, coastal and river waters frequently contaminated with sewage. Depth,
water temperature, precipitation, wind and salinity of the water in the mussel
and oyster growing area are important factors for the prediction of outbreak
risks. Shellfish has been reported to be important in the spread of foodborne
diseases in developed and developing countries. In Turkey, 78 tons of black
mussels per year are collected from sea for consumption. The presence of NoV in
mussels indicates that this shellfish could also be an important contaminant
for foodborne viral infections and outbreaks in Turkey. Monitoring the
prevalence of NoV in shellfish collected from Turkey can be used to prevent
outbreaks in touristic locations and to monitor the potential of Turkish seas
for viral contaminations. In this study, the role of shellfish in viral
gastroenteritis outbreaks associated with NoV and strategies for preventing virus
transmission via shellfish are reviewed.

Anahtar Kelimeler

Norovirus, Shellfish, Mussel, Oyster, Gastroenteritis

Kabuklu Deniz Ürünleri: Norovirüs Salgınları ve Sporadik Enfeksiyonlar İçin Risk

Öz

Daha önceleri Caliciviridae
familyasından Norwalk benzeri virüsler olarak bilinen norovirüler (NoV),
ikosahedral kapsid simetrisine sahip, zarfsız, pozitif (+) polariteli, tek
iplikli RNA virüsleridir. NoV enfeksiyonu hem sekretuar hem de osmotik ishale
neden olmaktadır. Enfeksiyonun meydana gelmesi için birkaç NoV partikülü
yeterli olmaktadır. NoV, esas olarak kontamine gıdalar ve su ile yayılmaktadır.
Virüsün yayılmasından kişiden kişiye doğrudan temas veya kontamine yüzeyler ve
kusmuk ile temas da sorumludur. Genel olarak, NoV kaynaklı epidemik ve pandemik
salgınlar görülmekte olup sporadik vakalar da bildirilmiştir. Salgınlar ve
sporadik enfeksiyonlar, NoV ile kontamine olmuş kabuklu deniz ürünleri (örneğin
midye, istiridye ve yengeç), yumuşak kırmızı meyveler (çilek ve ahududu), sebzeler
(marul, domates ve maydanoz), unlu mamuller, şarküteri ürünleri, salatalar,
sandviçler, su ve buzun tüketimi sonucunda meydana gelmektedir. NoV, dünya
çapında bakteriyel olmayan ishal vakalarının yarısından fazlasından sorumludur.
Midye ve istiridye gibi kabuklu deniz ürünlerinden kaynaklanan NoV salgınları
dünyada yaygın olarak görülmektedir. Virüs bulaşmış sularda yetiştirilen
kabuklu deniz ürünlerinin ve enfekte bireyler tarafından hazırlanan deniz ürünlerinin
salgınlarda rol oynayabileceği bildirilmektedir. Midye ve istiridye gibi çift
kabuklu/çenetli deniz ürünleri, beslenme faaliyetlerinin bir parçası olarak
büyük miktarlarda suyu filtreleyebilmekte ve bu nedenle sıklıkla kanalizasyonla
kontamine olmuş sığ, kıyı ve nehir sularındaki virüsleri biriktirip
yoğunlaştırabilmektedir. Derinlik, su sıcaklığı, yağış ve rüzgâr ile midye ve
istiridye yetiştirme alanlarındaki suyun tuzluluğu salgın risklerinin tahmini
için önemli faktörlerdir. Kabuklu deniz ürünlerinin gelişmiş ve gelişmekte olan
ülkelerde gıda kaynaklı hastalıkların yayılmasında önemli olduğu bildirilmektedir.
Türkiye'de tüketim için denizden yılda 78 ton kara midye avlanmaktadır. Toplanan
midyelerde NoV varlığı, bu kabuklu deniz ürününün Türkiye'de gıda kaynaklı
viral enfeksiyonlar ve salgınlar için önemli bir kontaminasyon kaynağı
olabileceğini göstermektedir. Ülkemizde avlanan kabuklu deniz ürünlerinde NoV
varlığının izlenmesi, turistik bölgelerdeki salgınların önlemesi ve Türk
denizlerinin viral kontaminasyon potansiyelinin izlemesi için kullanılabilir.
Bu çalışmada, NoV kaynaklı gastroenterit salgınlarında kabuklu deniz
ürünlerinin rolü ve kabuklu deniz ürünleri kaynaklı bulaşmaların önlemesinde
kullanılabilecek başlıca stratejiler derlenmiştir.

Anahtar Kelimeler

Norovirüs, Kabuklu deniz ürünü, Midye, İstiridye, Gastroenterit

Kaynakça

• [1] World Health Organization. (2017) Global Foodborne Infections Network. http://www.who/int/gfn/supported/en/ Erişim Tarihi: 10.05.2017.
• [2] Sözen, H., Gönen, I., Beydilli, H. (2014). An outbreak of norovirus gastroenteritis in a county in Turkey. Journal of Microbiology and Infectious Diseases, 4(1), 26-29.
• [3] Rodriguez-Lazaro, D., Cook, N., Ruggeri, F.M., Sellwood, J., Nasser, A., Nascimento, M. J., D'Agostino, M., Santos, R., Saiz, J.C., Rzeżutka, A., Bosch, A., Gironés, R., Carducci, A., Muscillo, M., Kovač, K., Diez-Valcarce, M., Vantarakis, A., von Bonsdorff, C.H., de Roda Husman, A.M., Hernández, M., van der Poel, W.M. (2012). Virus hazards from food water and other contaminated environments. FEMS Microbiology Reviews, 36(4), 786-814.
• [4] Centre for Disease Control and Prevention. (2017). Norovirus for public health professional. http://www.cdc.gov/norovirus/php/illness-outbreaks.html. Erişim tarihi: 18.04.2017
• [5] Erol, N., Delibaş, S.B., Özkoç, S., Ergüden, C., Aksoy, Ü. (2016). Investigation of parasitic and viral pathogens in mussels (Mytilus galloprovincialis) in the Gulf of Izmir, Turkey. Saudi Medical Journal, 37(6), 703-706.
• [6] Sağlık Bakanlığı (2018). https://www.saglik.gov.tr/TR,10488/bulasici-hastaliklar-surveyans-ve-kontrol-esaslari-yonetmeligi.html. Erişim tarihi: 12.06.2018.
• [7] Karst, S.M., Wobus, C.E., Lay, M., Davidson, J., Virgin, H.W. (2003). STAT1 Dependent innate immunity to a norwalk-like virus. Science, 299, 1575-78.
• [8] King, A.Q., Adams, M.J., Carstens, E.B., Lefkowits, E.J. ICTV Taxonomy History:Norwalk Virus. International Committee on Taxonomy of Viruses: http://www.data.ictvonline.org/proposals/Rarification_1998.pdf. Erişim Tarihi: 22.03.2017.
• [9] Stephanie, M.K., Zhu, S., Ian, G.G. (2015). The molecular pathology of noroviruses. Journal of Pathology, 235, 206-16.
• [10] Jiang, W., Wang, M., Wang, K., Estes, M.K. (1993). Sequence and genomic organization of norwalk virus. Virology, 195, 51-61.
• [11] Prasad, B.V., Hardy, M.E., Dokland, T., Bella, J., Rossmann, M.G., Estes, M.K. (1999). X-ray crystallographic structurevof the norwalk virus capsid. Science, 286(5438), 287-290.
• [12] Peasey, A.E., Ruiz-Palacios, G.M., Quigley, M., Newsholme, W., Martinez, J., Rosales, G., Jiang, X., Blumenthal, U.J. (2004). Seroepidemiology and risk factors for sporadic Norovirus/Mexico Strain. The Journal of Infectious Diseases, 189(11), 2027-2036.
• [13] Batten, C.A., Clarke, I.N., Kempster, S.L., Oliver, S.L., Bridger, J.C., Lambden, P.R. (2006). Characterization of a cross-reactive linear epitope in human genogroup I and bovine genogroup III norovirus capsid proteins. Virology, 356, 179–187.
• [14] Hall, A.J., Eisenbart, V.G., Etingue, A.L., Gould, L.H., Lopman, B.A., Parashar, U.D. (2014). Vital signs: Foodborne norovirus outbreaks - United States, 2009-2012. Morbidity and Mortality Weekly Report, 63(22), 491-495.
• [15] Karst, S.M., Zhu, S, Goodfellow, I.G. (2015). The molecular pathology of noroviruses. Journal of Pathology, 235, 206-216.
• [16] Zheng, D.P., Ando, T., Frankhauser, R.L., Beard, R.S., Glass, R.I., Monroe, S.S. (2006). Norovirus classification and proposed strain nomenclature. Virology, 346(2), 312-23.
• [17] Moshe, S.D. (2009). Is norovirus a foodborne or pandemic pathogen? An analysis of the transmission of Norovirus-associated gastroenteritis and the roles of food and food handlers dreyfuss. Foodborne Pathogens and Disease, 6(10), 1219-1228.
• [18] Brian, W.J., Mahy, V.M. (2005). Topley and Wilson’s Microbiology and Microbial Infections. 10th Ed. Hodder Arnold Company, London.
• [19] Kele, B. (2011). Comparative molecular genetic studies of nucleic acid detection in human noroviruses. Ph. Thesis. Albert Szent-Györgyi Clinical Center, Faculty of Medicine, University of Szeged: Institute of Clinical Microbiology.
• [20] Baldi, F., Bianco, M.A., Nardone, G., Pilotto, A., Zamparo, E. (2009). Focus on acute diarrhoeal disease. The World Journal of Gastroenterology, 15, 3341-3348.
• [21] Hodges, K., Gill, R. (2010) Infectious diarrhea: Cellular and molecular mechanisms. Gut Microbes, 1, 4-21.
• [22] Rockx, B., De Wit, M., Vennema, H., Vinje, J., De Bruin, E., Van Duynhoven, Y., Koopmans, M. (2002). Natural history of human calicivirus infection: a prospective cohort study. Clinical Infectious Diseases, 35, 246-253.
• [23] Lee, N., Chan, M.C., Wong, B., Choi, K.W., Sin, W., Lui, G., Chan, P.K., Lai, R.W., Cockram, C.S., Sung, J.J.Y., Leung, W.K. (2007). Fecal viral concentration and diarrhea in norovirus gastroenteritis. Emerging Infectious Diseases, 13, 1399-1401.
• [24] Levett, P.N., Gu, M., Luan, B., Fearson, M., Stubber, J., Jamieson, F., Petric, M. (1996). Longitudinal study of molecular epidemiology of small round-structured viruses in a pediatric population. Journal of Clinical Microbiology, 34, 1497-1501.
• [25] Centers for Disease Control and Prevention, (2002). Outbreak of acute gastroenteritis associated with Norwalk-like viruses among British military personnel-Afghanistan. Morbidity and Mortality Weekly Report, 51(22), 477-479.
• [26] Caul, E.O. (1994). Small round structured viruses: Airborne transmission and hospital control. Lancet, 343, 1240-1242.
• [27] Ushijima, H., Fujimoto, T., Müller, W.E., Hayakawa, S. (2014). Norovirus and foodborne disease: A rewiew. Food Safety, 2(3), 37-54.
• [28] Centre for Disease Control and Prevention. (2017). Norovirus. https://www.cdc.gov/norovirus/index.html. Erişim Tarihi: 08.04.2017.
• [29] Glass, I.R., Noel, J., Mitchell, D., Herrmann, J.E., Blacklow, N.R., Pickering, L.K., Dennehy, P., Ruiz-Palacios, G., de Guerrero, M.L., Monroe, S.S. (1996). The changing epidemiology of astrovirus-associated gastroenteritis: A review. Archives of Virology, 12, 287-300.
• [30] Haramoto, E., Katayama, H., Ohgaki, S. (2004). Detection of noroviruses in tap water in Japan by means of a new method for concentrating enteric viruses in large volumes of freshwater. Applied and Environmental Microbiology, 70, 2154-2160.
• [31] Scherer, K., Made, D., Ellerbroek, L., Schulenburg, J., Johne, R., Klein, G. (2009). Application of a swab sampling method fort he detection of norovirus and rotavirus on artificially contaminated food and environmental surfaces. Food and Environmental Virology, 1, 42-49.
• [32] Taku, A., Gulati, B.P., Allwood, P.B., Palazzi, K., Hedberg, C.W., Goyal, S.M. (2002), Concentration of caliciviruses from food contact surfaces. Journal of Food Protection, 65, 999-1004.
• [33] Teunis, P.F., Moe, C.L., Liu, P., Miller, S.E., Lindesmith, L., Baric, R.S., Le Pendu, J., Calderon, R.L. (2008). Norwalk virus: How infectious is it? Journal of Medical Viroogy, 80, 1468-1476.
• [34] Uyar, Y., Çarhan, A., Ozkaya, E., Ertek, M. (2008). Türkiye’de 2008 yılında ortaya çıkan ilk Norovirus salgınının laboratuvar sonuçlarının değerlendirilmesi. Mikrobiyoloji Bülteni, 42, 607-615.
• [35] Chung, J.Y. (2012). Noroviruses: Recent updates. Pediatric Gastroenterology, Hepatology & Nutrition, 15, 1-7.
• [36] Todd, E.C., Greig, J.D., Bartleson, C.A., Michaels, B.S. (2007). Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories. Journal of Food Protection, 70, 2199-2217.
• [37] Marks, P.J., Vipond, I.B., Carlisle, D., Deakin, D., Fey, R.E., Caul, E.O. (2000). Evidence for airborne transmission of Norwalk-like virus (NLV) in a hotel restaurant. Epidemiology Infection, 124, 481-487.
• [38] Prato, R., Lopalco, P.L., Chironna, M., Barbuti, G., Germinario, C., Quarto, M. (2004). Norovirus gastroenteritis general outbreak associated with raw shellfish consumption in South Italy. BMC Infectious Diseases, 4, 37.
• [39] Atmar, R.L., Estes, M.K., (2006). The epidemiologic and clinical importance of norovirus infection. Gastroenterology Clinics of North America, 35, 275-290.
• [40] Fankhauser, R.L., Monroe, S.S., Noel, J.S., Humphrey, C.D., Bresee, J.S., Parashar, U.D., Ando, T., Glass, R.I. (2002). Epidemiologic and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United States. The Journal of Infectious Diseases, 186, 1-7.
• [41] He, Z., Liu, B., Tao, Y., Li, C., Xia, M., Zhong, W., Jiang, X., Liu, H., Tan, M. (2017). Norovirus GII.17 natural infections in rhesus monkeys, China. Emerging Infectious Diseases, 23(2), 316-19.
• [42] Niendorf, S., Jacobsen, S., Faber, M., Eis-Hübinger, A.M., Hofmann, J., Zimmermann, O., Höhne, M., Bock, C.T. (2017). Steep rise in norovirus cases and emergence of a new recombinant strain GII.P16-GII.2, Germany, Winter 2016. Eurosurveillance, 22(4), 30447.
• [43] Siebenga, J.J., Vennema, H., Duizer, E., Koopmans, M.P. (2007). Gastroenteritis caused by norovirus GGII.4, The Netherlands, 1994-2005. Emerging Infectious Diseases, 13, 144-146.
• [44] T.C. Sağlık Bakanlığı Türkiye Halk Sağlığı Kurumu. (2017). Bulaşıcı Hastalıkların Tanısı için Saha Rehberi. http://mikrobiyoloji.thsk.saglik.gov.tr/ums/M-N/Norovirüs-enfeksiyonu.pdf. Erişim Tarihi: 03.05.2017.
• [45] Rydell, G.E. (2009). Norovirus, causative agent of winter vomiting disease, exploits several histo-blood group glycans for adhesion. Institute of Biomedicine Department of Clinical Chemistry and Transfusion Medicine University of Gothenburg, Intellecta Infolog AB, Västra Frölunda, 1-57p.
• [46] Treanor, J.J., Dolin, R. (2000). Norwalk virus and other Caliciviruses. Ed(s): Mandell, G.L., Bennett, J.E., Principles and practice of infectious diseases. 5th Edition, Churchhill Livingstone, Philadelphia, 1949-1956p.
• [47] Carlsson, B., Lindberg, A.M., Rodriguez-Diaz, J., Hedlund, K.O., Persson, B., Svensson, L. (2009). Quasispecies dynamics and molecular evolution of human norovirus capsid P region during chronic infection. Journal of General Virology, 90, 432-441.
• [48] Dimitriadis, A., Marshall, J.A. (2005). Evaluation of a commercial enzyme immunoassay for detection of norovirus in outbreak specimens. European Journal of Clinical Microbiology & Infectious Diseases, 24, 615-618.
• [49] Richards, A.F., Lopman, B., Gunn, A., Curry, A., Ellis, D., Cotterill, H., Ratcliffe, S., Jenkins, M., Appleton, H., Gallimore, C.I., Gray, J.J., Brown, D.W. (2003). Evaluation of a commercial ELISA for detecting Norwalk-like virus antigen in faeces. Journal of Clinical Virology, 26, 109-115.
• [50] Bucardo-Rivera, F. (2008). Pediatric Rotavirus and Norovirus Diarrhea in Nicaragua. Ph.D. Thesis. Department of Microbiology, Tumor and Cell Biology (MTC), Karolinska Institutet, Stockholm, Sweden. 1-71p.
• [51] Vinje, J.H., Vennema, L., Maunula, C.H., von Bonsdorff, M., Hoehne, E., Schreier, A., Richards, J., Green, D., Brown, S.S., Beard, S.S., de Bruin, M.E., Svensson, L., Koopmans, M.P. (2003). International collaborative study to compare 68 reverse transcriptase PCR assays for detection and genotyping of noroviruses. Journal of Clinical Microbiology, 41, 1423-1433.
• [52] Chang, K.O., Geroge, D.W. (2007). Interferons and ribavirin effectively inhibit Norwalk virus replication in replicon-bearing cells. Journal of Virology, 22, 12111-12118.
• [53] Dou, D., He, G., Mandadapu, S.R., Aravapali, S., Kim, Y., Chang, K.O., Groutas, E.C. (2012). Inhibition of noroviruses by piperazine derivatives. Bioorganic & Medicinal Chemistry Letters, 22, 377-379.
• [54] Barclay, L., Park, G.W., Vega, E., Hall, A., Parashar, U., Vinje, J., Lopman, B. (2014). Infection Control for Norovirus. Clinical Microbiology and Infection, 20, 731-40.
• [55] Baran, A., Erdogan, A. (2013). Gıda kaynaklı bir hastalık olarak norovirus salgınlarının önemi. Gıda, 38(2), 119-126.
• [56] Carter, M.J. (2005). Enterically infecting viruses; Pathogenicity, transmission and significance for food and waterborne infection. Journal of Applied Microbiology, 98, 1354-1380.
• [57] Guyader, F.S.L., Atmar, R.L., Le Pendu, J. (2012). Transmission of viruses through shellfish: when specific ligands come into play. Current Opinion in Virology, 2, 103-110.
• [58] Maalouf, H., Zakhour, M., Le Pendu,J., Le Saux, J.C., Atmar, R.L., Le Guyader, F.S. (2010). Distribution in tissue and seasonal variation of norovirus Genogroup I and II Ligands in oysters. Applied and Environmental Microbiology, 76(16), 5621-5630.
• [59] Woods, J.W., Calci, K.R., Marchant-Tambone, J.G., Burkhardt, W. (2016). Detection and molecular characterization of norovirus from oysters implicated in outbreaks in the US. Food Microbiology, 59, 76-84.
• [60] TÜİK (2018). www.tuik.gov.tr. Erişim Tarihi: 01.06.2018.
• [61] T.C. Gıda Tarım ve Hayvancılık Bakanlığı (2017). Veriler. https://www.tarim.gov.tr/sgb/Belgeler/SagMenuVeriler/BSGM.pdf. Erişim Tarihi: 04.06.2018
• [62] Bellou, M., Kokkinos, P., Vantarakis, A. (2012). Shellfish-borne viral outbreaks: A systematic review. Food and Environmental Virology, 4(4), 13-23.
• [63] Iwamoto, M., Ayers, T., Mahon, B.E., Swerdlow, D.L. (2010). Epidemiology of seafood-associated infections in the United States. Clinical Microbiology Reviews, 23(2), 399-411.
• [64] Campos, C.J.A., Lees, D.N. (2014). Environmental transmission of human noroviruses in shellfish waters. Applied and Environmental Microbiology, 80, 3552-3561.
• [65] Hassard, F., Sharp, J.H., Taft, H., LeVay, L., Harris, J.P., McDonald, J.E., Tuson, K., Wilson, J., Jones, D.L., Shelagh, K., Malham, S.K. (2017). Critical review on the public health impact of norovirus contamination in shellfish and the environment: A UK Perspective. Food and Environmental Virology, 9, 123–141.
• [66] Yilmaz, H., Bostan, K., Turan, N., Muratoglu, K., Yilmaz, A., Ozkul, A.A., Kocazeybek, B., Helps, C. (2010). Reall Time-PCR detection of norovirus in mussels collected from The Bosphorus in Istanbul, Turkey. Food and Environmental Virology, 2, 64.
• [67] Guyader, F.S.L., Bon, F., DeMedici, D., Parnaudeau, S., Bertone, A., Crudeli, S., Doyle, A., Zidane, M., Suffredini, E., Kohli, E., Maddalo, F., Monini, M., Gallay, A., Pommepuy, M., Pothier, P., Ruggeri, F.M. (2006). Detection of multiple noroviruses associated with an international gastroenteritis outbreak linked to oyster consumption. Journal of Clinical Microbiology, 44(11), 3878-3882.
• [68] Schaeffera, J., Le Sauxa, J.C., Loraa, M., Atmarb, R.L., Le Guyadera, F.S. (2013). Norovirus contamination on French marketed oysters. International Journal of Food Microbiology, 166(2), 244-248.
• [69] Verhoef, L., Hewitt, J., Barclay, L., Ahmed, S.M., Lake, R., Hall, A.J., Lopman, B., Kroneman, A., Vennema, H., Vinjé, J., Koopmans M. (2015). Norovirus genotype profiles associated with foodborne transmission, 1999-2012. Emerging Infectious Diseases, 21(4), 592-599.
• [70] Loury, P., Le Guyader, F.S., Le Saux, J.C., Ambert-Balay, K., Parrot, P., Hubert, B. (2015). A norovirus oyster-related outbreak in a nursing home in France, January 2012. Epidemiology & Infection, 143(12), 2486-93.
• [71] Cho, H.G., Lee, S.G., Lee, M.Y., Hur, E.S., Lee, J.S., Park, P.H., Park, Y.B., Yoon, M.H., Paik, S.Y. (2016). An outbreak of norovirus infection associated with fermented oyster consumption in South Korea, 2013. Epidemiology and Infection, 144(13), 2759-64.
• [72] Iizuka, S., Oka, T., Tabara, K., Omura, T., Katayama, K., Takeda, N., Noda, M. (2010). Detection of sapoviruses and noroviruses in an outbreak of gastroenteritis linked genetically to shellfish. Journal of Medical Virology, 82, 1247-1254.
• [73] De Medici, D., Croci, L., Suffredini, E., Toti, L. (2004). Reverse transcription-booster PCR for detection of noroviruses in shellfish. Applied and Environmental Microbiology, 70, 6329-6332.
• [74] EC (1991). European Directive 91/492. Laying down the health conditions for the production and the placing on the market of live bivalve molluscs. https://publications.europa.eu Erişim Tarihi: 1 Nisan 2018.
• [75] Le Guyader, F. S., Loisy, F., Atmar, R. L., Hutson, A. M., Estes, M. K., Ruvoen-Clouet, N. (2006). Norwalk virus-specific binding to oyster digestive tissues. Emerging Infectious Diseases, 12, 931-936.
• [76] Schwab, K.J., Neill, F.H., Estes, M.K., Metcalf, T.G. and Atmar, R.L. (1998) Distribution of Norwalk virus within shellfish following bioaccumulation and subsequent depuration by detection using RTPCR. Journal of Food Protection, 61, 1674-1680.
• [77] Polo, D., Álvarez, C., Díez, J., Darriba, S., Longa, A., Romalde, J.L. (2014). Viral elimination during commercial depuration of shellfish. Food Control, 43, 206-212.
• [78] Richards, G.P., McLeod, C., Le Guyader, F.S. (2010). Processing strategies to inactivate enteric viruses in shellfish. Food and Environmental Virology, 2(3), 183-193.
• [79] Lees, D. (2000). Viruses and bivalve shellfish. International Journal of Food Microbiology, 59, 81-116.
• [80] Hewitt, J., Greening, G.E. (2006). Effect of heat treatment on hepatitis A virus and norovirus in New Zealand greenshell mussels (Perna canaliculus) by quantitative real-time reverse transcription PCR and cell culture. Journal of Food Protection, 69, 2217-2223.
• [81] de Roda Husman, A. M., Bijkerk, P., Lodder, W., van den Berg, H., Pribil, W., Cabaj, A., Gehringer, P., Sommer, R., Duizer, E. (2004). Calicivirus inactivation by nonionizing (253.7-nanometer-wavelength [UV]) and ionizing (gamma) radiation. Applied and Environmental Microbiology, 70, 5089–5093.
• [82] Harewood, P., Rippey, S., Montesalvo, M. (1994). Effect of gamma irradiation on shelf life and bacterial and viral loads in hard-shelled clams (Mercenaria mercenaria). Applied and Environmental Microbiology, 60(7), 2666-2670.
• [83] Wang, J., Deng, Z. (2016). Modeling and prediction of oyster norovirus outbreaks along Gulf of Mexico coast. Environmental Health Perspectives, 124, 627-633.
• [84] Koopmans, M., Duizer, E. (2004). Foodborne viruses: an emerging problem. International Journal of Food Microbiology, 90(1), 23-41. [85] Yaprak, Ş.D. (2011). İmmünkompetan Erişkinler ve İmmünsupresif Tedavi Alanlarda Norovirus Enkefsiyonunun Araştırılması. Yüksek Lisans Tezi. Gaziantep Üniversitesi Sağlık Bilimleri Enstitüsü, Gaziantep.
• [86] Papafragkou, E., D’Souza, D.H., Jaykus, L.-A. (2006). Food-Borne Viruses: Prevention and Control. Viruses in Foods, First Edition. (Ed. Goyal, S.M.), Springer, USA, pp. 289-330.
• [87] Springthorpe, S., Sattar, S. (1998). Handwashing: what can we learn from recent research? Infection Control Today, 2, 20–28.