Abstract
Potential ways to address the issues that relate to the techniques for analyzing food and environmental samples for the presence of enteric viruses are discussed. It is not the authors’ remit to produce or recommend standard or reference methods but to address specific issues in the analytical procedures. Foods of primary importance are bivalve molluscs, particularly, oysters, clams, and mussels; salad crops such as lettuce, green onions and other greens; and soft fruits such as raspberries and strawberries. All types of water, not only drinking water but also recreational water (fresh, marine, and swimming pool), river water (irrigation water), raw and treated sewage are potential vehicles for virus transmission. Well over 100 different enteric viruses could be food or water contaminants; however, with few exceptions, most well-characterized foodborne or waterborne viral outbreaks are restricted to hepatitis A virus (HAV) and calicivirus, essentially norovirus (NoV). Target viruses for analytical methods include, in addition to NoV and HAV, hepatitis E virus (HEV), enteroviruses (e.g., poliovirus), adenovirus, rotavirus, astrovirus, and any other relevant virus likely to be transmitted by food or water. A survey of the currently available methods for detection of viruses in food and environmental matrices was conducted, gathering information on protocols for extraction of viruses from various matrices and on the various specific detection techniques for each virus type.
Similar content being viewed by others
References
Alexandersen S, Zhang Z, Reid SM, Hutchings GH, Donaldson AI (2002) J Gen Virol 83:1915
Al-Soud WA, Radstrom P (2001) J Clin Microbiol 39:485
American Public Health Association, American Water Works Association, Water Environment Federation (2005) In: Eaton AD et al (eds) Standard methods for the examination of water and wastewater, 21st edn. United Book Press, Baltimore, p 9
Arnal C, Crance JM, Gantzer C, Schwartzbrod L, Deloince R, Billaudel S (1998) Zentralbl Hyg Umweltmed 201:279
Atmar RL, Neill FH, Romalde JL et al (1995) Appl Environ Microbiol 61:3014
Backer H (2002) Clin Infect Dis 34:355
Baert L, Wobus CE, Van CE, Thackray LB, Debevere J, Uyttendaele M (2008a) Appl Environ Microbiol 74:543
Baert L, Uyttendaele M, Vermeersch M, Van CE, Debevere J (2008b) J Food Prot 71:1590
Bidawid S, Farber JM, Sattar SA (2000) J Virol Methods 88:175
Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, van der Noordaa J (1990) J Clin Microbiol 28:495
Booth TF, Kournikakis B, Bastien N et al (2005) J Infect Dis 191:1472
Branovic K, Forcic D, Ivancic J et al (2003) J Virol Methods 110:163
Burgener M, Candrian U, Gilgen M (2003) J Virol Methods 108:165
Burkhardt W III, Calci KR (2000) Appl Environ Microbiol 66:1375
Burton NC, Grinshpun SA, Reponen T (2007) Ann Occup Hyg 51:143
Butot S, Putallaz T, Sanchez G (2007) Appl Environ Microbiol 73:186
Butot S, Putallaz T, Sanchez G (2008) Int J Food Microbiol 126:30
Butot S, Putallaz T, Amoroso R, Sanchez G (2009) Appl Environ Microbiol 75:4155
Calder L, Simmons G, Thornley C et al (2003) Epidemiol Infect 131:745
Cannon RO, Poliner JR, Hirschhorn RB et al (1991) J Infect Dis 164:860
Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinje J (2006) J Food Prot 69:2761
Carducci A, Verani M, Casini B et al (2002) Lett Appl Microbiol 34:189
Carter MJ (2005) J Appl Microbiol 98:1354
Casas N, Amarita F, Martínez de Marañon I (2007) Int J Food Microbiol 120:179
Chancellor DD, Tyagi S, Bazaco MC et al (2006) J Food Prot 69:1468
Costafreda MI, Bosch A, Pintó RM (2006) Appl Environ Microbiol 72:3846
Cotterelle B, Drougard C, Rolland J, Becamel M, Boudon M, Pinede S, Traoré O, Balay K, Pothier P, Espié E (2005) Outbreak of norovirus infection associated with the consumption of frozen raspberries, France, March 2005. Euro Surveill 10(17):2690
Croci L, Dubois E, Cook N et al (2008) Food Anal Methods 1:73
Di Girolamo R, Liston J, Matches J (1977) Appl Environ Microbiol 33:19
Divizia M, Santi AL, Pana A (1989a) J Virol Methods 23:55
Divizia M, De Filippis P, Di Napoli A, Venuti A, Perez-Bercof R, Pana A (1989b) Water Res 23:1155
Dubois E, Hennechart C, Merle G et al (2007) Int J Food Microbiol 117:141
EPA, (U.S. Environmental Protection Agency, Cincinnati, 1984), Chap. Publication no. EPA/600/4-84-013
Falkenhorst G, Krusell L, Lisby M, Madsen SB, Böttiger BE, Mølbak K (2005) Imported frozen raspberries cause a series of norovirus outbreaks in Denmark, 2005. Euro Surveill 10(38):2795
Fell G, Boyens M, Baumgarte S (2007) Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 50:230
Fukuda S, Sasaki Y, Seno M (2008) Appl Environ Microbiol 74:3912
Gajardo R, Diez JM, Jofre J, Bosch A (1991) J Virol Methods 31:345
Garin D, Fuchs F, Crance JM et al (1994) Epidemiol Infect 113:541
Gassilloud B, Schwartzbrod L, Gantzer C (2003) Appl Environ Microbiol 69:3965
Gaulin CD, Ramsay D, Cardinal P, D’Halevyn MA (1999) Can J Public Health 90:37
Gerba CP (1987) In: Berg G (ed) Methods for recovering viruses from the environment. CRC Press, Boca Raton, p 1
Gilgen M, Germann D, Lüthy J, Hübner P (1997) Int J Food Microbiol 37:189
Grabow WOK, Taylor MB, Wolfaardt M (1996) WRC Report No. 496/1/96
Gutierrez-Aguirre I, Banjac M, Steyer A et al (2009) J Chromatogr A 1216:2700
Hedlund KO, Rubilar-Abreu E, Svensson L (2000) J Infect Dis 181:S275–S280
Hermann JR, Hoff SJ, Yoon KJ, Burkhardt AC, Evans RB, Zimmerman JJ (2006) Appl Environ Microbiol 72:4811
Hewitt J, Greening GE (2004) J Food Prot 67:1743
Hjertqvist M, Johansson A, Svensson N, Abom PE, Magnusson C, Olsson M, Hedlund KO, Andersson Y (2006) Four outbreaks of norovirus gastroenteritis after consuming raspberries, Sweden, June-August 2006. Euro Surveill 11(36):3038
Hogan CJ Jr, Kettleson EM, Lee MH, Ramaswami B, Angenent LT, Biswas P (2005) J Appl Microbiol 99:1422
Hoorfar J, Cook N (2003) Methods Mol Biol 216:51
Hoorfar J, Cook N, Malorny B et al (2003) J Clin Microbiol 41:5835
Hoorfar J, Malorny B, Abdulmawjood A, Cook N, Wagner M, Fach P (2004) J Clin Microbiol 42:1863
Houde A, Guevremont E, Poitras E et al (2007) J Virol Methods 140:80
Hourfar MK, Schmidt M, Seifried E, Roth WK (2005) Vox Sang 89:71
Hurst CJ, Reynolds KA (2002) In: Hurst CJ et al (eds) Manual of environmental microbiology, 2nd edn. ASM Press, Washington, p 244
Hutin YJ, Pool V, Cramer EH et al (1999) N Engl J Med 340:595
Johnston MV (2000) J Mass Spectrom 35:585
Jothikumar N, Aparna K, Kamatchiammal S, Paulmurugan R, Saravanadevi S, Khanna P (1993) Appl Environ Microbiol 59:2558
Jothikumar N, Lowther JA, Henshilwood K, Lees DN, Hill VR, Vinje J (2005) Appl Environ Microbiol 71:1870
Knepp JH, Geahr MA, Forman MS, Valsamakis A (2003) J Clin Microbiol 41:3532
Kobayashi S, Natori K, Takeda N, Sakae K (2004) Microbiol Immunol 48:201
Kok T, Wati S, Bayly B, Devonshire-Gill D, Higgins G (2000) J Clin Virol 16:59
Koopmans M, Duizer E (2004) Int J Food Microbiol 90:23
Korsager B, Hede S, Bøggild H, Böttiger BE, Mølbak K (2005) Two outbreaks of norovirus infections associated with the consumption of imported frozen raspberries, Denmark, May-June 2005. Euro Surveill 10(25):2729
Kovac K, Gutierrez-Aguirre I, Banjac M et al (2009) J Virol Methods 162:272
Kramberger P, Petrovic N, Strancar A, Ravnikar M (2004) J Virol Methods 120:51
Lamhoujeb S, Fliss I, Ngazoa SE, Jean J (2008) Appl Environ Microbiol 74:3349
Lawson HW, Braun MM, Glass RI et al (1991) Lancet 337:1200
Le Guyader FS, Neill FH, Dubois E et al (2003) Int J Food Microbiol 87:107
Le Guyader FS, Mittelholzer C, Haugarreau L et al (2004) Int J Food Microbiol 97:179
Le Guyader FS, Bon F, DeMedici D et al (2006a) J Clin Microbiol 44:3878
Le Guyader F, Loisy F, Atmar RL et al (2006b) Emerg Infect Dis 12:931
Le Guyader FS, Le Saux JC, Ambert-Balay K et al (2008) J Clin Microbiol 46:4011
Le Guyader FS, Parnaudeau S, Schaeffer J et al (2009) Appl Environ Microbiol 75:618
Lodder-Verschoor F, de Roda Husman AM, van den Berg HH, Stein A, van Pelt-Heerschap HM, van der Poel WH (2005) J Food Prot 68:1853
Mattison K, Brassard J, Gagne MJ et al (2009) Int J Food Microbiol 132:73
Maunula L, Miettinen IT, von Bonsdorff CH (2005) Emerg Infect Dis 11:1716
Meinhardt PL (2006) J Water Health 4:27
Menut C, Beril C, Schwartzbrod L (1993) Water Sci Technol 27:294
Milne SA, Gallacher S, Cash P, Lees DN, Henshilwood K, Porter AJ (2007) J Food Prot 70:1475
Moore BE, Sagik BP, Sorber CA (1979) Appl Environ Microbiol 38:688
Murray CJ (2002) In: Hurst CJ et al (eds) Manual of environmental microbiology, 2nd edn. ASM, Washington, p 166
Nasser A, Weinberg D, Dinoor N, Fattal B, Adin A (1995) Water Sci Technol 31:63
Nishida T, Nishio O, Kato M et al (2007) Microbiol Immunol 51:177
Niu MT, Polish LB, Robertson BH et al (1992) J Infect Dis 166:518
Nuanualsuwan S, Cliver DO (2002) J Virol Methods 104:217
Nuanualsuwan S, Cliver DO (2003) Appl Environ Microbiol 69:350
Oron G, Goemanns M, Manor Y, Feyen J (1995) Water Res 29:1069
Passagot J, Crance JM, Deloince R, Laveran H, Beytout D, Fontanges R (1985) Water Res 19:1167
Perelle S, Cavellini L, Burger C et al (2009) J Virol Methods 157:80
Pintó RM, Diez JM, Bosch A (1994) J Med Virol 44:310
Pintó RM, Gajardo R, Abad FX, Bosch A (1995) Environ Sci Technol 29:2636
Pintó RM, Costafreda MI, Bosch A (2009) Appl Environ Microbiol 75:7350
Ponka A, Maunula L, von Bonsdorff C-H, Lyytikainen O (1999) Euro Surveill 4:66
Pyankov OV, Agranovski IE, Pyankova O et al (2007) Environ Microbiol 9:992
Ramsay CN, Upton PA (1989) Lancet 1:43
Reid TM, Robinson HG (1987) Epidemiol Infect 98:109
Reynolds KA, Gerba CP, Abbaszadegan M, Pepper LL (2001) Can J Microbiol 47:153
Richards GP, Watson MA, Kingsley DH (2004) J Virol Methods 116:63
Rodriguez RA, Pepper IL, Gerba CP (2009) Appl Environ Microbiol 75:297
Rodriguez-Lazaro D, D’Agostino M, Pla M, Cook N (2004) J Clin Microbiol 42:5832
Rodriguez-Lazaro D, Pla M, Scortti M, Monzo HJ, Vazquez-Boland JA (2005) Appl Environ Microbiol 71:9008
Rodríguez-Lázaro D, Lombard B, Smith H et al (2007) Trends Food Sci Technol 18:306
Rutjes SA, Italiaander R, van den Berg HH, Lodder WJ, Roda Husman AM (2005) Appl Environ Microbiol 71:3734
Rutjes SA, Lodder-Verschoor F, van der Poel WH, van Duijnhoven YT, de Roda Husman AM (2006a) J Food Prot 69:1949
Rutjes SA, van den Berg HH, Lodder WJ, Roda Husman AM (2006b) Appl Environ Microbiol 72:5349
Rzezutka A, Alotaibi M, D’Agostino M, Cook N (2005) J Food Prot 68:1923
Sanchez G, Bosch A, Pintó RM (2007) Lett Appl Microbiol 45:1
Scherer K, Mäde D, Ellerbroek L, Schulenburg J, Johne R, Klein G (2009) Food Environ Virol 1:42
Schwab KJ, De Leon R, Sobsey MD (1993) Water Sci Technol 27:211
Schwab KJ, Neill FH, Le Guyader F, Estes MK, Atmar RL (2001) Appl Environ Microbiol 67:742
Senouci S, Maul A, Schwartzbrod L (1996) Zentralbl Hyg Umweltmed 198:307
Shan XC, Wolffs P, Griffiths MW (2005) Appl Environ Microbiol 71:5624
Soule H, Genoulaz O, Gratacap-Cavallier B, Chevallier P, Liu JX, Seigneurin JM (2000) Water Res 34:1063
Taylor MB, Cox N, Vrey MA, Grabow WOK (2001) Water Res 35:2653
Tian P, Mandrell R (2006) J Appl Microbiol 100:564
Topping JR, Schnerr H, Haines J et al (2009) J Virol Methods 156:89
Urbanucci A, Myrmel M, Berg I, von Bonsdorff CH, Maunula L (2009) Int J Food Microbiol 135:175
Van Heerden J, Ehlers MM, Van Zyl WB, Grabow WOK (2004) Water Sci Technol 50:39
Van Heerden J, Ehlers MM, Heim A, Grabow WOK (2005) J Appl Microbiol 99:234
van Zyl WB, Williams PJ, Grabow WOK, Taylor MB. (2004) Application of a molecular method for the detection of group A rotaviruses in raw and treated water. Water Sci Technol 50:223–228
Van Zyl WB, Page NA, Grabow WOK, Steele AD, Taylor MB (2006) Appl Environ Microbiol 72:4554
Venter JME. (2004) The incidence of hepatitis A virus in selected water sources and associated risk of infection in South Africa. [MSc dissertation]. Pretoria: University of Pretoria
Verreault D, Moineau S, Duchaine C (2008) Microbiol Mol Biol Rev 72:413
Vilaginès P, Sarrette B, Husson G, Vilaginès R (1993) Water Sci Technol 27:306
Vilaginès P, Sarrette B, Champsaur H et al (1997) Water Sci Technol 35:445
Vivancos R, Shroufi A, Sillis M et al (2009) Int J Infect Dis 13:629
Vivier JC, Ehlers MM, Grabow WOK (2001) Water Res 38:2699
Vivier JC, Ehlers MM, Grabow WOK, Havelaar AH (2002) Water Supply 2:1
Vivier JC, Ehlers MM, Grabow WOK (2004) Water Res 38:11
Widdowson MA, Sulka A, Bulens SN et al (2005) Emerg Infect Dis 11:95
Williams FP, Fout GS (1992) Environ Sci Technol 26:689
Wyn-Jones P (2007) In: Bosch A (ed) Human viruses in water. Elsevier, Amsterdam, p 177
Acknowledgments
This paper was produced in a cooperative action of the working group on analytical methods of the EU COST action 929 (Environet). G. Sánchez is the recipient of a JAE doctor grant from the “Consejo Superior de Investigaciones Científicas” (CSIC). Rembuluwani Netshikweta acknowledges a post-graduate bursary from the Poliomyelitis Research Foundation, South Africa.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bosch, A., Sánchez, G., Abbaszadegan, M. et al. Analytical Methods for Virus Detection in Water and Food. Food Anal. Methods 4, 4–12 (2011). https://doi.org/10.1007/s12161-010-9161-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12161-010-9161-5
Keywords
Profiles
- Gloria Sánchez View author profile
- Annalaura Carducci View author profile