Various types of surfaces are used today in the food industry, such as plastic, stainless steel, glass, and wood. These surfaces are subject to contamination by microorganisms responsible for the cross-contamination of food by contact with working surfaces. The HACCP-based processes are now widely used for the control of microbial hazards to prevent food safety issues. This preventive approach has resulted in the use of microbiological analyses of surfaces as one of the tools to control the hygiene of products. A method of recovering microorganisms from different solid surfaces is necessary as a means of health prevention. No regulation exists for surface microbial contamination, but food companies tend to establish technical specifications to add value to their products and limit contamination risks. The aim of this review is to present the most frequently used methods: swabbing, friction or scrubbing, printing, rinsing or immersion, sonication and scraping or grinding and describe their advantages and drawbacks. The choice of the recovery method has to be suitable for the type and size of the surface tested for microbiological analysis. Today, quick and cheap methods have to be standardized and especially easy to perform in the field.
References
[1]
Mariani, C.; Briandet, R.; Chamba, J.F.; Notz, E.; Carnet-Pantiez, A.; Eyoug, R.N.; Oulahal, N. Biofilm ecology of wooden shelves used in ripening the French raw milk smear cheese Reblochon de Savoie. J. Dairy Sci. 2007, 90, 1653–1661, doi:10.3168/jds.2006-190.
[2]
Gullo, M.; De Vero, L.; Giudici, P. Acetobacter pasteurianus selected strain and acetic acid bacteria species succession in traditional balsamic vinegar. Appl. Environ. Microbiol. 2009, 75, 2585–2589, doi:10.1128/AEM.02249-08.
[3]
Gill, C.O.; McGinnis, J.C. Contamination of beef trimmings with Escherichia coli during a carcass breaking process. Food Res. Int. 2000, 33, 125–130, doi:10.1016/S0963-9969(00)00026-0.
[4]
Allen, V.M.; Bull, S.A.; Corry, J.E.L.; Domingue, G.; J?rgensen, F.; Frost, J.A.; Whyte, R.; Gonzalez, A.; Elviss, N.; Humphrey, T.J. Campylobacter spp. contamination of chicken carcasses during processing in relation to flock colonisation. Int. J. Food Microbiol. 2007, 113, 54–61, doi:10.1016/j.ijfoodmicro.2006.07.011.
[5]
Escherichia coli O157:H7 Outbreak linked to home-cooked hamburger—California, July 1993. MMWR, 1994, 43, pp. 213–216. Available online: http://www.cdc.gov/mmwr/preview/mmwrhtml/00026029.htm (accessed on 5 November 2013).
Beuchat, L.R. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 2002, 4, 413–423, doi:10.1016/S1286-4579(02)01555-1.
[9]
Arthur, T.M.; Bosilevac, J.M.; Brichta-Harhay, D.M.; Kalchayanand, N.; King, D.A.; Shackelford, S.D.; Wheeler, T.L.; Koohmaraie, M. Source tracking of Escherichia coli O157:H7 and Salmonella contamination in the lairage environment at commercial U.S. beef processing plants and identification of an effective intervention. J. Food Protect. 2008, 71, 1752–1760.
[10]
Berends, B.R.; Van Knapen, F.; Mossel, D.A.A.; Burt, S.A.; Snijders, J.M.A. Salmonella spp. on pork at cutting plants and at the retail level and the influence of particular risk factors. Int. J. Food Microbiol. 1998, 44, 207–217, doi:10.1016/S0168-1605(98)00122-6.
[11]
Berends, B.R.; Van Knapen, F.; Mossel, D.A.A.; Burt, S.A.; Snijders, J.M.A. Impact on human health of Salmonella spp. on pork in The Netherlands and the anticipated effects of some currently proposed control strategies. Int. J. Food Microbiol. 1998, 44, 219–229, doi:10.1016/S0168-1605(98)00121-4.
[12]
McLauchlin, J. The relationship between Listeria and listeriosis. Food Control 1996, 7, 187–193, doi:10.1016/S0956-7135(96)00038-2.
[13]
Vogel, B.F.; Hansen, L.T.; Mordhorst, H.; Gram, L. The survival of Listeria monocytogenes during long term desiccation is facilitated by sodium chloride and organic material. Int. J. Food Microbiol. 2010, 140, 192–200, doi:10.1016/j.ijfoodmicro.2010.03.035.
[14]
Wenger, J.D.; Swaminathan, B.; Hayes, P.S.; Green, S.S.; Pratt, M.; Pinner, R.W.; Schuchat, A.; Broome, C.V. Listeria monocytogenes contamination of turkey franks: Evaluation of a production facility. J. Food Protect. 1990, 53, 1015–1019.
[15]
Peccio, A.; Autio, T.; Korkeala, H.; Rosmini, R.; Trevisani, M. Listeria monocytogenes occurrence and characterization in meat-producing plants. Lett. Appl. Microbiol. 2003, 37, 234–238, doi:10.1046/j.1472-765X.2003.01384.x.
[16]
Règlement (CE) N° 852/2004 du parlement Européen et du conseil du 29 Avril 2004 relatif à l'hygiène des denrées alimentaires. Available online: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2004:226:0003:0021:FR:PDF (accessed on 5 November 2013).
[17]
Annex 1. Recommendations for an environmental monitoring programme for Listeria monocytogenes in processing areas. Guidelines on the Application of General Principles of Food Hygiene to the Control of Listeria monocytogenes in Ready-to-Eat Foods, pp. 1–28. Available online: http://www.codexalimentarius.org/standards/list-of-standards/ (accessed on 5 November 2013).
[18]
Carpentier, B.; Barre, L. Guidelines on Sampling the Food Processing Area and Equipment for the Detection of Listeria monocytogenes; French Agency for Food, Environmental and Occupational Health Safety: Maisons-Alfort, France, 2012; pp. 1–15. Available online: http://ec.europa.eu/food/food/biosafety/salmonella/docs/guidelines_sampling_en.pdf (accessed on 5 November 2013).
[19]
Hirsch, P.; Eckhardt, F.E.W.; Palmer, R.J. Methods for the study of rock-inhabiting microorganisms—A mini review. J. Microbiol. Methods 1995, 23, 143–167, doi:10.1016/0167-7012(95)00017-F.
[20]
Carpentier, B. Sanitary quality of meat chopping board surfaces: A bibliographical study. Food Microbiol. 1997, 14, 31–37, doi:10.1006/fmic.1996.0061.
[21]
Giudici, P.; Gullo, M.; Solieri, L.; Falcone, P.M. Technological and microbiological aspects of traditional Balsamic vinegar and their influence on quality and sensorial properties. Adv. Food Nutr. Res. 2009, 58, 137–182, doi:10.1016/S1043-4526(09)58004-7.
[22]
Angelotti, R.; Foter, M.J.; Buschand, K.A.; Lewis, K.H. A comparative evaluation of methods for determining the bacterial contamination of surfaces. J. Food Sci. 1958, 23, 175–185, doi:10.1111/j.1365-2621.1958.tb17556.x.
[23]
Moore, G.; Griffith, C. A comparison of surface sampling methods for detecting coliforms on food contact surfaces. Food Microbiol. 2002, 19, 65–73, doi:10.1006/fmic.2001.0464.
[24]
Microbiology of Food and Animal Feeding Stuffs—Horizontal Methods for Sampling Techniques from Surfaces Using Contact Plates and Swabs; ISO 18593:2004; ISO: Geneva, Switzerland, 2004.
[25]
Bodur, T.; Cagri-Mehmetoglu, A. Removal of Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 biofilms on stainless steel using scallop shell powder. Food Control 2012, 25, 1–9, doi:10.1016/j.foodcont.2011.09.032.
[26]
Lortal, S.; Di Blasi, A.; Madec, M.-N.; Pediliggieri, C.; Tuminello, L.; Tanguy, G.; Fauquant, J.; Lecuona, Y.; Campo, P.; Carpino, S.; Licitra, G. Tina wooden vat biofilm: A safe and highly efficient lactic acid bacteria delivering system in PDO Ragusano cheese making. Int. J. Food Microbiol. 2009, 132, 1–8.
[27]
Pérez-Rodríguez, F.; Valero, A.; Carrasco, E.; García, R.M.; Zurera, G. Understanding and modelling bacterial transfer to foods: A review. Trends Food Sci. Technol. 2008, 19, 131–144, doi:10.1016/j.tifs.2007.08.003.
[28]
Notermans, S.; Hindle, V.; Kampelmacher, E.H. Comparison of cotton swab versus alginate swab sampling method in the bacteriological examination of broiler chickens. J. Hyg. Camb. 1976, 77, 205–210, doi:10.1017/S0022172400024633.
[29]
Davidson, C.A.; Griffith, C.J.; Peters, C.A.; Fielding, L.M. Evaluation of two methods for monitoring surface cleanliness-ATP bioluminescence and traditional hygiene swabbing. Luninescence 1999, 14, 33–38, doi:10.1002/(SICI)1522-7243(199901/02)14:1<33::AID-BIO514>3.0.CO;2-I.
[30]
Miller, A. Wooden and polyethylene cutting boards: potential for the attachment and removal of bacteria from ground beef. J. Food Protect. 1996, 59, 854–859.
[31]
Higgins, M. A comparison of the recovery rate of organisms from cotton-wool and calcium alginate wool swabs. Bull. Minist. Hlth. Publ. Hlth. Lab. Serv. 1950, 9, 50–51.
[32]
Mahony, J.B.; Chernesky, M.A. Effect of swab type and storage temperature on the isolation of Chlamydia trachomatis from clinical specimens. J. Clin. Microbiol. 1985, 22, 865–867.
[33]
Hodges, L.R.; Rose, L.J.; Peterson, A.; Noble-Wang, J.; Arduino, M.J. Evaluation of a macrofoam swab protocol for the recovery of Bacillus anthracis spores from a steel surface. Appl. Environ. Microbiol. 2006, 72, 4429–4430, doi:10.1128/AEM.02923-05.
[34]
Asséré, A.; Oulahal, N.; Carpentier, B. Comparative evaluation of methods for counting surviving biofilm cells adhering to a polyvinyl chloride surface exposed to chlorine or drying. J. Appl. Microbiol. 2008, 104, 1692–1702, doi:10.1111/j.1365-2672.2007.03711.x.
[35]
Osterblad, M.; Jarvinen, H.; Lonnqvist, K.; Huikko, S.; Laippala, P.; Viljanto, J.; Arvilommi, H.; Huovinen, P. Evaluation of a new cellulose sponge-tipped swab for microbiological sampling: A laboratory and clinical investigation. J. Clin. Microbiol. 2003, 41, 1894–1900, doi:10.1128/JCM.41.5.1894-1900.2003.
[36]
Montville, R.; Chen, Y.; Schaffner, D.W. Risk assessment of hand washing efficacy using literature and experimental data. Int. J. Food Microbiol. 2002, 73, 305–313, doi:10.1016/S0168-1605(01)00666-3.
[37]
Yamaguchi, N.; Ishidoshiro, A.; Yoshida, Y.; Saika, T.; Senda, S.; Nasu, M. Development of an adhesive sheet for direct counting of bacteria on solid surfaces. J. Microbiol. Meth. 2003, 53, 405–410, doi:10.1016/S0167-7012(02)00246-4.
[38]
Brown, G.S.; Betty, R.G.; Brockmann, J.E.; Lucero, D.A.; Souza, C.A.; Walsh, K.S.; Boucher, R.M.; Tezak, M.; Wilson, M.C.; Rudolph, T. Evaluation of a wipe surface sample method for collection of Bacillus spores from nonporous surfaces. Appl. Environ. Microbiol. 2007, 73, 706–710, doi:10.1128/AEM.01082-06.
[39]
Hall, L.; Hartnett, M.J. Measurement of the bacterial contamination on surfaces in hospitals. Public Health Rep. 1964, 79, 1021–1024, doi:10.2307/4592309.
[40]
Cervenka, L.; Kristlova, J.; Peskova, I.; Vytrasova, J.; Pejchalova, M.; BrozkovaI, V. Persistence of Arcobacter butzleri CCUG 30484 on plastic, stainless steel and glass surfaces. Braz. J. Microbiol. 2008, 39, 517–520, doi:10.1590/S1517-83822008000300021.
[41]
Khamisse, E.; Firmesse, O.; Christieans, S.; Chassaing, D.; Carpentier, B. Impact of cleaning and disinfection on the non-culturable and culturable bacterial loads of food-contact surfaces at a beef processing plant. Int. J. Food Microbiol. 2012, 158, 163–168, doi:10.1016/j.ijfoodmicro.2012.07.014.
[42]
Niskanen, A.; Pohja, M.S. Comparative studies on the sampling and investigation of microbial contamination of surfaces by the contact plate and swab methods. J. Appl. Microbiol. 1977, 42, 53–63, doi:10.1111/j.1365-2672.1977.tb00669.x.
[43]
Peneau, S.; Chassaing, D.; Carpentier, B. First evidence of division and accumulation of viable but nonculturable Pseudomonas fluorescens cells on surfaces subjected to conditions encountered at meat processing premises. Appl. Environ. Microbiol. 2007, 73, 2839–2846, doi:10.1128/AEM.02267-06.
[44]
EHEDG. A method for assessing the in-place cleanability of food-processing equipment. Food Sci. Technol. 2007, 18, S54–S58, doi:10.1016/j.tifs.2006.11.021.
[45]
Ak, N.O.; Cliver, D.O.; Kaspar, C.W. Cutting boards of plastic and wood contaminated experimentally with bacteria. J. Food Protect. 1994, 57, 16–22.
[46]
McEvoy, J.M.; Nde, C.W.; Sherwood, J.S.; Logue, C.M. An evaluation of sampling methods for the detection of Escherichia coli and Salmonella on turkey carcasses. J. Food Protect. 2005, 68, 34–39.
[47]
Oliva, A.; Nguyen, B.L.; Mascellino, M.T.; D’Abramo, A.; Iannetta, M.; Ciccaglioni, A.; Vullo, V.; Mastroianni, C.M. Sonication of explanted cardiac implants improves microbial detection in cardiac device infections. J. Clin. Microbiol. 2013, 51, 496–502, doi:10.1128/JCM.02230-12.
[48]
Portillo, M.E.; Salvadó, M.; Trampuz, A.; Plasencia, V.; Rodriguez-Villasante, M.; Sorli, L.; Puig, L.; Horcajada, J.P. Sonication versus vortexing of implants for diagnosis of prosthetic joint infection. J. Clin. Microbiol. 2013, 51, 591–594, doi:10.1128/JCM.02482-12.
[49]
Puig-Verdié, L.; Alentorn-Geli, E.; González-Cuevas, A.; Sorlí, L.; Salvadó, M.; Alier, A.; Pelfort, X.; Portillo, M.E.; Horcajada, J.P. Implant sonication increases the diagnostic accuracy of infection in patients with delayed, but not early, orthopaedic implant failure. Bone Joint J. 2013, 95-B, 244–249, doi:10.1302/0301-620X.95B2.30486.
[50]
Mettler, E.; Carpentier, B. Hygienic quality of floors in relation to surface texture. Food Bioprod. Process. 1999, 77, 90–96, doi:10.1205/096030899532376.
[51]
Le Bayon, I.; Callot, H.; Kutnik, M.; Denis, C.; Revol-Junelles, A.-M.; Millière, J.-B.; Giraud, M.; Gabillé, M.; Passédat, N. Development of Microbiological Test Methods for the Wooden Packaging of Foodstuffs; The International Research Group on Wood Protection: Biarritz, France, 2010.
Kang, D.; Eifert, J.; Williams, R.; Pao, S. Evaluation of quantitative recovery methods for Listeria monocytogenes applied to stainless steel. J. AOAC Int. 2007, 90, 810–817.
[54]
Vainio-Kaila, T.; Kyyhkynen, A.; Viitaniemi, P.; Siitonen, A. Pine heartwood and glass surfaces: Easy method to test the fate of bacterial contamination. Eur. J. Wood Wood Prod. 2010, 69, 391–395.
[55]
Zangerl, P.; Matlschweiger, C.; Dillinger, K.; Eliskases-Lechner, F. Survival of Listeria monocytogenes after cleaning and sanitation of wooden shelves used for cheese ripening. Eur. J. Wood Wood Prod. 2010, 68, 415–419, doi:10.1007/s00107-009-0381-6.
[56]
Mamlouk, D.; Hidalgo, C.; Torija, M.-J.; Gullo, M. Evaluation and optimisation of bacterial genomic DNA extraction for no-culture techniques applied to vinegars. Food Microbiol. 2011, 28, 1374–1379, doi:10.1016/j.fm.2011.06.009.
[57]
Krysinski, E.P.; Brown, L.J.; Marchisello, T.J. Effect of cleaners and sanitizers on Listeria monocytogenes attached to product contact surfaces. J. Food Protect. 1992, 55, 246–251.
[58]
Lauzon, H.L. The Suitability of Materials Used in the Food Industry, Involving Direct or Indirect Contact with Food Products. Project P 98076 “Wood in the Food Industry”; Nordic Industrial Fund, Center for Innovation and Commercial Development and the Industry Partners in Denmark, Iceland, Norway and Sweden, 1998, p. 5. Available online: http://www.fefpeb.org/attachments/036_000513_Report1.pdf (accessed on 5 November 2013).
[59]
Midelet, G.; Carpentier, B. Transfer of microorganisms, including Listeria monocytogenes, from various materials to beef. Appl. Environ. Microbiol. 2002, 68, 4015–4024, doi:10.1128/AEM.68.8.4015-4024.2002.
[60]
Carpentier, B. La qualité hygiénique des surfaces de découpe de viande: étude bibliographique. Viandes et Produits Carnés 1997, 18, 114–118.
[61]
Oulahal-Lagsir, N.; Martial-Gros, A.; Boistier, E.; Blum, L.J.; Bonneau, M. The development of an ultrasonic apparatus for the non-invasive and repeatable removal of fouling in food processing equipment. Lett. Appl. Microbiol. 2000, 30, 47–52, doi:10.1046/j.1472-765x.2000.00653.x.
[62]
Revol-Junelles, A.-M.; Miguindou-Mabiala, R.; Roger-Maigné, D.; Millière, J.-B. Behavior of Escherichia coli cells and Bacillus cereus spores on Poplar wood crates by impedance measurements. J. Food Protect. 2005, 68, 80–84.
[63]
Carpentier, B.; Cerf, O. Review—Persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 2011, 145, 1–8, doi:10.1016/j.ijfoodmicro.2011.01.005.
[64]
Chasseignaux, E.; Gérault, P.; Toquin, M.-T.; Salvat, G.; Colin, P.; Ermel, G. Ecology of Listeria monocytogenes in the environment of raw poultry meat and raw pork meat processing plants. FEMS Microbiol. Lett. 2002, 210, 271–275, doi:10.1111/j.1574-6968.2002.tb11192.x.
[65]
Pearson, L.J.; Marth, E.H. Listeria monocytogenes—Threat to a safe food supply: A Review. J. Dairy Sci. 1990, 73, 912–928, doi:10.3168/jds.S0022-0302(90)78748-6.
[66]
Veulemans, A.; Jacqmain, E.; Jacqmain, D. Etude d’une méthode simple pour la détermination du degré de pollution des surfaces et la comparaison du pouvoir désinfectant de divers produits d’entretien. Rev. Ferment. Ind. Aliment 1970, 25, 58–65.
[67]
Bae, Y.-M.; Baek, S.-Y.; Lee, S.-Y. Resistance of pathogenic bacteria on the surface of stainless steel depending on attachment form and efficacy of chemical sanitizers. Int. J. Food Microbiol. 2012, 153, 465–473, doi:10.1016/j.ijfoodmicro.2011.12.017.
[68]
Scott, E.; Bloomfield, S.F. The survival and transfer of microbial contamination via cloths, hands and utensils. J. Appl. Microbiol. 1990, 68, 271–278, doi:10.1111/j.1365-2672.1990.tb02574.x.
[69]
Jiang, X.; Doyle, M.P. Fate of Escherichia coli O157:H7 and Salmonella Enteritidis on currency. J. Food Protect. 1999, 62, 805–807.
[70]
Kusumaningrum, H.D.; Riboldi, G.; Hazeleger, W.C.; Beumer, R.R. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int. J. Food Microbiol. 2003, 85, 227–236, doi:10.1016/S0168-1605(02)00540-8.
[71]
Haeghebaert, S.; Le Querrec, F.; Vaillant, V.; Delarocque Astagneau, E.; Bouvet, P. Les toxi-infections alimentaires collectives en France en 1998. Bull. Epidemiol. Hebdomadaire, 2001. Available online: http://www.invs.sante.fr/beh/2001/15/beh_15_2001.pdf (accessed on 13 November 2013).
[72]
Reuter, M.; Mallett, A.; Pearson, B.M.; van Vliet, A.H.M. Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl. Environ. Microbiol. 2010, 76, 2122–2128, doi:10.1128/AEM.01878-09.
[73]
Barnes, L.-M.; Lo, M.F.; Adams, M.R.; Chamberlain, A.H.L. Effect of milk proteins on adhesion of bacteria to stainless steel surfaces. Appl. Environ. Microbiol. 1999, 65, 4543–4548.