Virus recovering from strawberries: Evaluation of a skimmed milk organic flocculation method for assessment of microbiological contamination

International Journal of Food Microbiology

Volumn 217, Issue , 2016, Pages 14-19

  Melgaço, Fabiana Gil ^a   Victoria, Matias ^b   Corrêa, Adriana Abreu ^c   Ganime, Ana Carolina ^a   Malta, Fábio Correia ^d   Brandão, Marcelo Luiz Lima ^e   de Mello Medeiros, Valéria ^e   de Oliveira Rosas, Carla ^e   Bricio, Silvia Maria Lopes ^e   Miagostovich, Marize Pereira ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^d FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^e National Institute for Quality Control in Health   (Brazil)

Author keywords

Enteric virus; Foodborne; Low cost; Skimmed milk flocculation method; Strawberry

Indexed keywords

GENOMIC DNA; VIRUS RNA; MACROGOL DERIVATIVE; VIRUS DNA;

ADENOVIRIDAE; ARTICLE; BACTERIUM IDENTIFICATION; ELUTION; ENTERIC VIRUS; FECAL COLIFORM; FILTRATION; FLOCCULATION; FOOD CONTAMINATION; FOOD INDUSTRY; GENOTYPE; HUMAN ADENOVIRUS C; LIMIT OF DETECTION; LISTERIA MONOCYTOGENES; MILK; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRECIPITATION; PROCESS CONTROL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA; STRAWBERRY; VIRAL CONTAMINATION; VIRUS DETECTION; ANALYSIS; ANIMAL; CHEMISTRY; DNA SEQUENCE; ENTEROVIRUS; EVALUATION STUDY; FECES; FOOD CONTROL; FRAGARIA; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; VIROLOGY;

ADENOVIRUSES, HUMAN; ANIMALS; BASE SEQUENCE; DNA, VIRAL; ENTEROVIRUS; FECES; FLOCCULATION; FOOD CONTAMINATION; FOOD MICROBIOLOGY; FRAGARIA; HUMANS; LISTERIA MONOCYTOGENES; MILK; NOROVIRUS; POLYETHYLENE GLYCOLS; RNA, VIRAL; SALMONELLA; SEQUENCE ANALYSIS, DNA;

EID: 84944415943     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2015.10.005     Document Type: Article

References (51)

1. Allard A., Albinsson B., Wadell G. Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. J. Clin. Microbiol. 2001, 39(2):498-505.
2. Anvisa Agência Nacional de Vigilância Sanitária, Ministério da Saúde. Resolução RDC n.°12, de 2 de janeiro de 2001. Aprova regulamento Técnico sobre Padrões Microbiológicos para alimentos e seus anexos I e II 2001, 45. Diário Oficial da União, Poder Executivo, Brasília-DF, Brasil, (n.7-E, 10 jan. 2001. Seção1).
3. Anvisa Agência Nacional de Vigilância Sanitária, Ministério da Saúde, Brasil. Unidade Técnica de Doenças de Veiculação Hídrica e Alimentar - UHA, Coordenação Geral de Doenças Transmissíveis - CGDT, Secretaria de Vigilância em Saúde - SVS. Dados Epidemiológicos - DTA período de 2000 a 2014 2014, (Available from: http://portal.saude.gov.br/portal/saude/profissional/area.cfm?id_area=1550. Accessed 2014 September 1).
4. Atreya C.D. Major foodborne illness causing viruses and current status of vaccines against the diseases. Foodborne Pathog. Dis. 2004, 1(2):89-96.
5. Baert L., Wobus C.E., Coillie E.V., Thackray L.B., Debevere J., Uyttendaele M. Detection of murine norovirus 1 by using plaque assay, transfection assay, and real-time reverse transcription-PCR before and after heat exposure. Appl. Environ. Microbiol. 2008, 74(2):543-546.
6. Baert L., Uyttendaele M., Debevere J. 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. Int. J. Food Microbiol. 2008, 123:101-108.
7. Bofill-Mas S., Rusiñol M., Fernandez-Cassi X., Carratalà A., Hundesa A., Girones R. Quantification of human and animal viruses to differentiate the origin of the fecal contamination present in environmental samples. BioMed Res. Int. 2013, (2013, Article ID 192089).
8. Brandão M.L.L., Almeida D.O., Bispo F.C.P., Bricio S.M.L., Marin V.A., Miagostovich M.P. Assessment of microbiological contamination of fresh, minimally processed, and ready-to-eat lettuces (Lactuca sativa), Rio de Janeiro State, Brazil. J. Food Sci. 2014, 79(5):M961-M966.
9. Brassard J., Gagné M.J., Généreux M., Côté C. Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries. Appl. Environ. Microbiol. 2012, 78(10):3763-3766.
10. Calgua B., Mengewein A., Grunert A., Bofill-Mas S., Clemente-Casares P., Hundesa A., Wyn-Jones A.P., López-Pila J.M., Girones R. Development and application of a one-step low cost procedure to concentrate viruses from seawater samples. J. Virol. Methods 2008, 153(2):79-83.
11. Comelli H.L., Rimstad E., Larsen S., Myrmel M. Detection of norovirus genotype I.3b and II.4 in bioaccumulated blue mussels using different virus recovery methods. Int. J. Food Microbiol. 2008, 127:53-59.
12. de Abreu Corrêa A., Miagostovich M.P. Optimization of an adsorption-elution method with a negatively charged membrane to recover norovirus from lettuce. Food Environ. Virol. 2013, 5(3):144-149.
13. Demeke T., Jenkins G.R. Influence of DNA extraction methods, PCR inhibitors and quantification methods on real-time PCR assay of biotechnology-derived traits. Anal. Bioanal. Chem. 2010, 396(6):1977-1990.
14. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
15. Feng P., Weagant S.D., Grant M.A., Burkhardt W. Enumeration of Escherichia coli and the Coliform Bacteria. Bacteriological Analytical Manual Online 2002, (Chapter 4. [S.l]; FDA. [Accessed 2014 July 26]. Available from: [http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm064948.htm]).
16. Fioretti J.M., Ferreira M.S., Victoria M., Vieira C.B., Xavier M.P., Leite J.P., Miagostovich M.P. Genetic diversity of noroviruses in Brazil. Mem. Inst. Oswaldo Cruz 2011, 106(8):942-947.
17. Fumian T.M., Leite J.P., Marin V.A., Miagostovich M.P. A rapid procedure for detecting noroviruses from cheese and fresh lettuce. J. Virol. Methods 2009, 5(1):39-43.
18. Fumian T.M., Vieira C.B., Leite J.P., Miagostovich M.P. Assessment of burden of virus agents in an urban sewage treatment plant in Rio de Janeiro, Brazil. J. Water Health 2013, 11(1):110-119.
19. Greening G.H. Human and Animal Viruses in food (Including Taxonomy of Enteric Viruses). Viruses in Foods 2006, 345. (Chapter 2). S. Goyal, Hardcover (Eds.).
20. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
21. Hernroth B.E., Conden-Hansson A.C., Rehnstam-Holm A.S., Girones R., Allard A.K. Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilus edulis: the first Scandinavian report. Appl. Environ. Microbiol. 2002, 68:4523-4533.
22. Hewitt J., Greening G.E., Leonard M., Lewis G.D. Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Int. J. Food Microbiol. 2013, 167:177-185.
23. Hitchins A.D., Jinneman K. Detection and Enumeration of Listeria monocytogenes in Foods. Bacteriological Analytical Manual Online, Chapter 10 2011, ([S.l]; FDA. [Accessed 2014 July 26]. Available from: [http://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm071400.htm]).
24. Kageyama T., Kojima S., Shinohara M., Uchida K., Fukushi S., Hoshino F.B., Takeda N., Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 2003, 41:1548-1557.
25. Koopmans M., Von Bonsdorff C.-H., Vinjé J., De Medici D., Monroe S. Foodborne viruses. FEMS Microbiol. Rev. 2002, 26:187-205.
26. Kramer A., Schwebke I., Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BioMed Cent. Infect. Dis. 2006, 6(130).
27. Laidler M.R., Tourdjman M., Buser G.L., Hostetler T., Repp K.K., Leman R., Samadpour M., Keene W.E. Escherichia coli O157:H7 infections associated with consumption of locally grown strawberries contaminated by deer. Clin. Infect. Dis. 2013, 57(8):1129-1134.
28. Mäde D., Trübner K., Neubert E., Höhne M., Johne R. Detection and typing of norovirus from frozen strawberries involved in a large-scale gastroenteritis outbreak in Germany. Food Environ. Virol. 2013, 5:162-168.
29. Maunula L., Roivainen M., Keränen M., Mäkela S., Söderberg K., Summa M., von Bonsdorff C.H., Lappalainen M., Korhonen T., Kuusi M., Niskanen T. Detection of human norovirus from frozen raspberries in a cluster of gastroenteritis outbreaks. Rapid Commun. Eurosurveillance 2009, 14(49):19435.
30. Maunula L., Kaupke A., Vasickova P., Söderberg K., Kozyra I., Lazic S., van der Poel W.H.M., Bouwknegt M., Rutjes S., Willems K.A., Moloney R., D'Agostino M., Husman A.M.R.H., von Bonsdorff C.-H., Pavlik A.R.I.P., Petrovic T., Cook N. Tracing enteric viruses in the European berry fruit supply chain. Int. J. Food Microbiol. 2013, 167:177-185.
31. Miagostovich M.P., Ferreira F.F., Guimarães F.R., Fumian T.M., Diniz-Mendes L., Luz S.L., Silva L.A., Leite J.P. Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, Central Amazonia, Brazil. Appl. Environ. Microbiol. 2008, 74(2):375-382.
32. Morales-Rayas R., Wolffs P.F.G., Griffiths M.W. Anion-exchange filtration and real-time PCR for the detection of a norovirus surrogate in food. J. Food Prot. 2009, 72:2178-2183.
33. Painter J.A., Hoekstra R.M., Ayers T., Tauxe R.V., Braden C.R., Angulo F.J., Griffin P.M. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998-2008. Emerg. Infect. Dis. 2013, 19(3):407-415.
34. Park Y., Cho Y.H., Jee Y., Ko G. Immunomagnetic separation combined with real-time reverse transcriptase PCR assays for detection of norovirus in contaminated food. Appl. Environ. Microbiol. 2008, 74:4226-4230.
35. Pina S., Puig M., Lucena F., Jofre J., Girones R. Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Appl. Environ. Microbiol. 1998, 64(9):3376-3382.
36. Richards G.P. Enteric virus contamination of foods through industrial practices: a primer on intervention strategies. J. Ind. Microbiol. Biotechnol. 2001, 27(2):117-125.
37. Rodriguez-Manzano J., Hundesa A., Calgua B., Carratala A., Maluquer de Motes C., Rusiñol M., Moresco V., Ramos A.P., Martínez-Marca F., Calvo M., Monte Barardi C.R., Girones R., Bofill-Mas S. Adenovirus and norovirus contaminants in commercially distributed shellfish. Food Environ. Virol. 2013, 6(1):31-41.
38. Rzezutka A., Alotaibi M., D'Agostino M., Cook N. A centrifugation-based method for extraction of norovirus from raspberries. J. Food Prot. 2005, 68(9):1923-1925.
39. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 14(4):406-425.
40. Stals A., Baert L., Van Coillie E., Uyttendaele M. Evaluation of a norovirus detection methodology for soft red fruits. Food Microbiol. 2011, 28:52-58.
41. Stals A., Baert L., Van Coillie E., Uyttendaele M. Extraction of food-borne viruses from food samples: a review. Int. J. Food Microbiol. 2012, 153:1-9.
42. Summa M., von Bonsdorff C.H., Maunula L. Evaluation of four virus recovery methods for detecting noroviruses on fresh lettuce, sliced ham, and frozen raspberries. J. Virol. Methods 2012, 183:154-160.
43. Szymczak B., Szymczak M., Sawicki W., Dabrowski W. Anthropogenic impact on the presence of L. monocytogenes in soil, fruits, and vegetables. Folia Microbiol. 2014, 59:23-29.
44. Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol. Biol. Evol. 1992, 14:678-687.
45. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
46. Victoria M., Fumian T.M., Rocha M.S., Dalmao F., Leite J.P., Girones R., Miagostovich M.P. Gastroenteric virus dissemination and influence of rainfall events in urban beaches in Brazil. J. Appl. Microbiol. 2014, 117(4):1210-1218.
47. Vinje J. Advances in laboratory methods for detection and typing of noroviruses. J. Clin. Microbiol. 2015, 53(2):373-381.
48. Wobus C.E., Thackray L.B., Virgin H.W. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 2006, 80(11):5104-5112.
49. Wyn-Jones A.P., Carducci A., Cook N., D'Agostino M., Divizia M., Fleischer J., Gantzer C., Gawler A., Girones R., Holler C., de Roda Husman A.M., Kay D., Kozyra I., Lopez-Pila J., Muscillo M., Nascimento M.S., Papageorgiou G., Rutjes S., Sellwood J., Szewzyk R., Wyer M. Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res. 2011, 45(3):1025-1038.
50. Yin J.L., Shackel N.A., Zekry A., McGuinness P.H., Richards C., Putten K.V., McCaughan G.W., Eris J.M., Bishop G.A. Real-time reverse transcriptase-polymerase chain reaction (RT-PCR) for measurement of cytokine and growth factor mRNA expression with fluorogenic probes or SYBR green I. Immunol. Cell Biol. 2001, 79(3):213-221.
51. Zheng D.P., Ando T., Fankhauser R.L., Beard R.S., Glass R.I., Monroe S.S. Norovirus classification and proposed strain nomenclature. Virology 2006, 346:312-323.