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Biofilm formation in dairy, fish processing, poultry, meat, and ready-to-eat foods industries are discussed. Biofilm renders its inhabitants resistant to antimicrobial agents and cleaning. Conventional and emergent control strategies used to efficiently maintain good hygiene throughout food industries is discussed.
Biofilm formation in dairy, fish processing, poultry, meat, and ready-to-eat foods industries are discussed. Biofilm renders its inhabitants resistant to antimicrobial agents and cleaning. Conventional and emergent control strategies used to efficiently maintain good hygiene throughout food industries is discussed.
Biofilm formation in dairy, fish processing, poultry, meat, and ready-to-eat foods industries are discussed. Biofilm renders its inhabitants resistant to antimicrobial agents and cleaning. Conventional and emergent control strategies used to efficiently maintain good hygiene throughout food industries is discussed.
Svabic- Vlahovic, 2003). The biolm formation is a stepwise and dynam- ical process consisting of (i) initial attachment, (ii) irreversible attachment, (iii) early development of biolm architecture, (iv) maturation, and (v) dispersion (Fig. 1). 2.1. Initial attachment The bacterias initial attachment can be active or passive, depending on their motility or the gravitational transportation of their planktonic (free oating), diffusion or shear force of the surrounding uid phase (Kumar &Anand, 1998). The cells adhesion during this process strongly depends on the physiochemical prop- erties of the bacterial cell surface (Ferreira, Pereira, &Melo, 2010). At rst, the adherent cells, those that originate biolm formation on a surface, possess only a small quantity of extracellular polymeric substance (EPS) and many are capable of independent movement (OToole & Kolter, 1998) by pilus-mediated twitching or gliding motility. In this stage, the adhesion is reversible since the attached microorganisms are not yet committed to the differentiation processda series of morphological changesdwhichleads to biolm formation, and many of the cells may detach from the surface and return to the planktonic lifestyle (Stoodley, Sauer, Davies, & Costerton, 2002). The surface properties also play an important role in bacterial adhesion. Generally, any surface is vulnerable to biolm develop- ment including plastic, glass, metal, wood, and food products. The adhesion to the surface is also dependent upon the physicochemical properties of the surface such as texture (rough or smooth) (Donlan, 2002), surface charge (Abdallah, Chaieb, Zmantar, Kallel, &Bakhrouf, 2009), hydrophobicity (Donlan, 2002), pH, temperature (Nilsson, Ross, & Bowman, 2011), and nutrient composition of the pre- conditioning solution (Donlan, 2002; Gerstel & Rmling, 2001). For instance, the research of Sinde and Carballo (2000) found that Salmonella and Listeria can attach in a higher numbers to hydro- phobic surfaces thanthe hydrophilic ones. Furthermore, the surfaces overlaid by a so-called conditioning lm comprising macromole- cules, such as organic substances, will enhance the attachment of bacterial cells (Tang, Flint, Bennett, Brooks, & Morton, 2009). It has Fig. 1. Stages of biolms development. This diagram is a cartoon of the 5 stages of biolm development: 1 reversible attachment, 2 irreversible attachment, 3 early development of biolm architecture, 4 maturation and 5 nally dispersion. Under the cartoon are 5 electron micrographs showing what the biolm actually looks like at each stage. Image by D. Davis from Monroe, D Looking for chinks in the armor of bacterial biolms PLoS Biol, Vol. 5, issue 11. S. Srey et al. / Food Control 31 (2013) 572e585 573 also been shown that any pre-existing EPS will facilitate the adhe- sion (Flemming & Schaule, 1988). 2.2. Irreversible attachment The change from reversible to irreversible attachment is a shift from a weak interaction of the bacteria with the surface to a permanent bonding with the presence of EPS (Stoodley, Sauer, et al., 2002). After irreversible attachment, strong shear force or chemical breaking of the attachment forces by enzymes, deter- gents, surfactants, sanitizers (Sinde & Carballo, 2000), and/or heat is needed for biolm removal (Augustin, Ali-Vehmas, & Atroshi, 2004; Maukonen et al., 2003; Sinde & Carballo, 2000). Gerke, Kraft, Sssmuth, Schweitzer, and Gtz (1998) worked on Staphylococcus epidermis and has shown that adherent bacteria produce a poly- saccharide intercellular adhesion that bonds the cells together and facilitates microcolony formation and biolm maturation. 2.3. Early development of biolm architecture (microcolony formation) Microcolony formation results from concurrent accumulation and growth of microorganisms and is associated with the produc- tion of EPS (Chmielewski & Frank, 2003), which helps strengthen the bond between the bacteria and the substratum and stabilizes the colony from any environmental stress (Donlan, 2002). Studies of bacterial species in natural systems have shown that accumu- lation could embrace the recruitment of planktonic cells from the surrounding medium as a result of cell-to-cell communication (quorum sensing) (McLean, Whiteley, Stickler, & Fuqua, 1997; Pesci et al., 1999). OToole and Kolter (1998) indicated that in order to allow microcolony formation of Pseudomonas aeruginosa PA14 to take place type IV pili are required. Swimming motility was considered to enable the microorganisms to overcome repulsive forces at the surfaceewater interface, allowing them to reach the substratum and form microcolonies by twitching motility powered by extension and retraction of type IV pili (Skerker & Berg, 2001). Microcolonies can be very benecial as they provide interspecies substrate exchange and/or mutual end-product removal to bacteria (Costerton, Lewandowski, Debeer, Caldwell, & Korber, 1994). 2.4. Maturation The biolm maturation is the step where it develops into an organized structure which can be at or mushroom-shaped (Fig. 2), depending on the nutrient source it is reliant upon (Chmielewski & Frank, 2003; Klausen et al., 2003). In order to reach structural maturity, periods of 10 days or more are required (Stoodley, Sauer, et al., 2002). Bacteria grow under sessile form in heterogeneous complex-enclosed microcolonies scattered with open water chan- nels (Davey & OToole, 2000). In a study, the mature biolms was evaluated and compared with chemostat cultures of P. aeruginosa by DNA microarray technology (Whiteley et al., 2001). The study showed that over 70 genes were altered, including genes encoding proteins involved in translation, metabolism, membrane transport and/or secretion, and gene regulation. 2.5. Dispersion Dispersion is the last step in the biolm formation cycle, and it allows the cells to revert into their planktonic form (Sauer, Camper, Ehrlich, Costerton, & Davies, 2002). External perturbation, such as increased uid shear (Stoodley, Cargo, Rupp, Wilson, & Klapper, 2002), internal biolm processes, such as endogenous enzymatic degradation, or the release of EPS or surface-binding protein, are all possible causes of biolm detachment (Kaplan, Ragunath, Ramasubbu, & Fine, 2003; Kaplan, Ragunath, Velliyagounder, Fine, & Ramasubbu, 2004). Detachment seems to be an active process which allows for the colonization of new niches (Sauer et al., 2002). In addition, starvation is also considered as a reason of detachment and allows bacteria to search for a nutrient-rich environment (OToole & Kaplan, 2000). Other researchers have also proposed the involvement of enzymatic activity in the degradation of EPS. For instance, the production of surface protein releasing enzyme dispersin B that degrades the biolms of Staphylococcus epidermidis is found in the Actinobacillus actinomycetemcomitans (Kaplan et al., 2004). Another study indicates that biolms can be removed from surfaces by gentle rinsing if there is an overexpression of alginate lyase which would cause the degradation of alginate. 3. Biolm formation 3.1. Biolm forming strength The ability to formbiolmvaries greatly not just betweenspecies. Even in the same species with different strains and serovars, biolm formation strength can vary signicantly. For instance, in a study on the ability of ve Salmonella enterica serovars to attach to and colo- nize intact and cut lettuce and cabbage surfaces (Patel & Sharma, 2010) showed that S. enterica serovars Tennessee and Thompson can produce considerably more biolm than serovars Braenderup, Negev, and Newport; and could be considered as strong biolm formers according to the criteria suggested by Stepanovic et al. (2004). In another work, Listeria monocytogenes Scott A and 3990 were known to be high biolm producers, while L. monocytogenes strains YM96 and 303 were moderate biolm producers and L. monocytogenes 17 was the least productive biolm former (Chmielewski & Frank, 2006). However, there are also other factors that inuence biolm forming capacity, specically surface proper- ties and nutrient availability. Salmonella spp. and L. monocytogenes Fig. 2. SEM images of biolm formation on polystyrene coupons in A. hydrophila. S. Srey et al. / Food Control 31 (2013) 572e585 574 strains preferably adhere to hydrophobic surface materials (Donlan, 2002). Furthermore, biolmproductionof Bacillus cereus onstainless steel coupons at the aireliquidinterface was foundto be thicker than that in submerged systems (Wijman, de Leeuw, Moezelaar, Zwietering, & Abee, 2007). Similarly, Staphylococcus isolated from food andfoodprocessing environments was studied, and the biolm was thicker with the presence of sodium chloride or glucose (Mretr et al., 2003). It has also been speculated that carbohydrate metabolismmay have aneffect onbiolmproductionamongvarious gram-positive bacteria (Pillai et al., 2004). As can be seen, biolm formationcapacityvaries betweengenera, species, andstrains, andit is inuenced by other factors such that one type of bacteria can be a strong biolm producer under a certain environment and become weak in another environment. 3.2. Food contact surface materials for biolm formation Besides bacteria genus and species, extrinsic factors also play a major role inuencing the degree of attachment and biolm formation. Materials that make up food contact surfaces were postulated to have a large effect on the level of attachment and bio- lm formation. The materials used for food contact surfaces are knowntobestainless steel, glass, rubber, polyurethane(Chia, Goulter, McMeekin, Dykes, & Fegan, 2009), Teon, nitrile butyl rubber (NBR, Buna-n) (Storgards, Simola, Sjberg, & Wirtanen, 1999), and wooddfor developing countries (Mariani et al., 2011). Stepanovic et al. (2004) reported that Salmonella spp. and L. monocytogenes can produce high biolms on plastic surfaces. In another study, the surface roughness of a polyesterurethane conveyor belt was reported to have a signicant inuence on the biolm forming ability of L. monocytogenes. Even the weak strains demonstrated the ability to formbiolmandcouldnot totallybeeliminated(Chaturongkasumrit, Takahashi, Keeratipibul, Kuda, & Kimura, 2011). Adetunji and Isola (2011) studied the biolm formation on wood, stainless steel, and glass surfaces, with the results demonstrating that wood encourages biolm formation due to its porosity and absorbency, which can entrap organic material and bacteria. The authors stated that glass is the preferred food contact surface owing to its smooth surface and corrosion resistant properties, while stainless steel can resist the impact damage better but it is vulnerable to corrosion. Chia et al. (2009) found that Salmonella attached the best to Teon, followed by stainless steel and glass, then Buna-n and polyurethane. It is suggested that the adhering cells depend on the interfacial free energies of the surface. Their results suggested that surface rough- ness has no correlation with adhesion, while many other authors have stated the opposite (Howell & Behrends, 2006; Scardino, Harvey, & De Nys, 2006). It has been speculated that the difference between the degree of surface roughness studied depends on a subjective assessment (e.g. polishedor unpolished), whichcouldbe the reason for the different observations (Chia et al., 2009). Corre- spondingly, Arnold, Boothe, Suzuki, and Bailey (2004) reported that there were dramatically less bacterial cells attached to electro- polished stainless steel compared to an untreated stainless steel surface. It was also suggested that besides the material itself other hygienic design such as welding, joints, corners, and equipment design could also be an important factor affecting biolm formation (Gubjrnsdttir, Einarsson, & Thorkelsson, 2005). 4. Biolm: problems in food industry 4.1. Produce industry Currently, microbial control strategies are not efcient enough to provide a complete eradication of hazardous microorganisms without affecting product qualities (FAO/WHO, 2008, p. 151). It is documented that the safety of prolonging the shelf life of fresh-cut produce depends on the washing step, while the efcacy of sani- tizers on produce can only reduce at most 2 log of bacteria; the microorganisms presumably are protected by their location in the plant tissue (internalized, in stomata, cracks, crevices, cut surfaces), and/or by biolms produced by the microbes themselves (Whipps, Hand, Pink, & Bending, 2008). Trimming, cutting, washing, rinsing, dewatering and packaging are all used in produce industry and are considered to be the primary source of cross-contamination (Suslow, 2001). Lpez-Glvez, Gil, Truchado, Selma, and Allende (2010) investigated the effect of subsequent washing with chlo- rine or sodium hypochlorite on short-term cross-contaminated fresh-cut lettuce. The results indicated that subsequent sanitation steps cannot efciently inactivate Escherichia coli cells on the vegetable tissue. Through scanning electron microscopy, bacteria cells were detected in clusters or tissue stomata (Fig. 3) where they are considered as protected fromdisinfectants, which could explain the inefciency of disinfecting solutions. However, chlorine dioxide and sodium hypochlorite solutions were able to inactivate a large portion of E. coli cells that were transferred from an inoculated sample to wash water. It has been suggested that the use of sani- tation solutions may be able to reduce cross-contamination between clean and contaminated produce during the washing process. It is recommended that disinfectants should be used in order to avoid cross-contamination from contaminated produce to clean produce (Keskinen, Burke, & Annous, 2009; Lpez-Glvez et al., 2010). Produces are generally consumed raw, hence packingdthe last step of processingdis considered as one of the critical control points. This last step should be controlled attentively and regularly to avoid re-contamination. It has been observed that 12.3% of all foodborne outbreaks from 1990 to 2007 were related to fresh produce whereas 10% caused by improper handling post harvesting from farm and the rest were associated with growing, packing, shipping or processing of fresh produce (Alliance For Food and Fig. 3. Attachment of A. hydrophila on iceberg lettuce stomata grown at 25
C for 24 h. S. Srey et al. / Food Control 31 (2013) 572e585 575 Farming, 2010). In 2011, there was an outbreak linked to whole cantaloupe contaminated with L. monocytogenes (Caron 2011). It is speculated that the root cause of the outbreaks is the unsanitary condition of the packing shed. Moreover, the microorganisms were also found other places include the conveyor belt, drying area and oor drain (Neuman, 2011). It is supposed that pathogens become rmly attached in inaccessible place (Neuman, 2011) and form biolm then internalize within the produce (Sapers, 2001). Microorganisms are found to preferentially attach to intact surfaces of produce (Liao & Cooke, 2001). Gandhi, Golding, Yaron, and Matthews (2001) found evidence of bacteria at a depth of 12 mm within intact alfalfa sprout tissue. In another study by Han, Sherman, Linton, Nielsen, and Nelson (2000), it was noticed that there was no remarkable growth of E. coli O157:H7 found on uninjured green pepper surfaces after inoculation and incubation for 24 h at 37
C; while signicant growth and multiplication was found on intact surfaces. Sanitizers such as ozone, chlorine, and organic acid were reported to be ineffective against microbial biolm(lmez & Temur, 2010). Furthermore, E. coli was reported to have survived a 20,000 ppm chlorine soak and grew to a level of 6 log CFU/g radish sprouts, which is remarkably higher than the initial count on the seeds. It was demonstrated that bacteria were generally detected in the roots of radish sprouts and all across the surface, and the cells are found to be located in biolms attached to radish sprout tissues during sprouting (Fransisca, Zhou, Park, & Feng, 2011). Hydrogen peroxide is also relatively ineffective in E. coli 766 elimination on cantaloupes; it was observed to be reduced by less than 1 log. Furthermore, immersion of cantaloupes in 1% hydrogen peroxide for 2 h did not show any increase in efcacy. It is speculated that this inefcacy is a result of the oxidation of the agents on the melon surface or from access to endogenous catalase (Sapers & Sites, 2003). 4.2. Dairy industry Milk is a very perishable product and is truly vulnerable to contamination by various microorganisms. The major sources of contaminated milk and milk products are usually considered to come from improperly cleaned and sanitized equipment (Jessen & Lammert, 2003; Koutzayiotis, 1992). It is well documented that the bacteria frequently encountered in the dairy environment belong to the genus Enterobacter (Salo, Ehavald, Raaska, Vokk, & Wirtanen, 2006), Listeria (Waak et al., 2002), Lactobacillus, Micro- coccus, Streptococcus, Bacillus (Sharma & Anand, 2002) and Pseu- domonas (Wiedmann, Weilmeier, Dineen, Ralyea, & Boor, 2000). In 2011, there was a recall of approximately 20 pounds of raw milk distributed in Washington state due to L. monocytogenes contami- nation (Anonymous, 2011). It is speculated that the type of bacteria in the milk samples may have shown biolm formation. For instance, the larger the amount of thermoduric Streptococci and Bacillus species in pasteurized milk compared to raw milk could be caused by the contamination of the dispersion of biolm (Flint, Bremer, & Brooks, 1997). To date, there are many studies focused on the various bacteria in dairy factories. Several studies (Mafu, Roy, Goulet, & Magny, 1990; Vanhaecke et al., 1990) have indicated that there is no correlation between surface irregularities or roughness and the bacteria attachment ability. However, Latorre et al. (2010) con- ducted a study on the presence of L. monocytogenes-containing biolm in milking equipment as a potential source of contamina- tion on a dairy farm. After having obtained positive results, electron microscopy scanning of the equipment showed the presence of individual and clusters of bacteria, and it was postulated that it was mainly associated with scratched surfaces. In another study, attachment and biolm formation by L. monocytogenes on stainless steel (SS, type 304, no. 4 nish) and Buna-n rubber (BN, acrylonitrile butadiene, 70 durometer), which are commonly used in food processing equipment, was evaluated (Helke, Somers, &Wong, 1993). According to the results, lactose had no effect on the attachment on either surface compared to the control PBS, while other compounds showed a signicance effect on the attachment. The authors suggested that the repulsion between negatively charged proteins and bacterial cell surfaces could to some extent provide an explanation for the decrease in attachment. A similar study demonstrated that in the presence of pasteurized whole milk with a relative humidity (RH) of 75%, L. monocytogenes endured on the BN surface between 25
C and 6
C, and 6
C on the SS surface and growing at 25
C on the SS surface, both at the same RH. At the same time, the attached cells decreased over time and the slowest rate of decrease was at 6
C and 75.5% (Helke & Wong, 1994). It was also documented that the BN surface had an inhibitory effect on the growth of L. monocytogenes and several other foodborne pathogens (Helke & Wong, 1994; Ronner & Wong, 1993). According to Ronner and Wong (1993), this inhibitory effect varies depending on the nutrient contents in the environment and at one-fth the amount of tryptose-phosphate broth nutrients, there is an increase in lag time. However, the effect can endure about 20 cycles of Clean-In-Place (CIP) (Helke & Wong, 1994). Furthermore, it was suggested that a slow growth rate could improve resistance to antimicrobial agents (Anwar, Dasgupta, & Costerton, 1990), which can to some extent explain why biolms on BN are more resistant to sanitizers than normally formed biolms (Wong, 1998). Biolm formation depends on many factors in dairy industry. Dairy products are very susceptible to contamination by biolms and it is challenging to eliminate those microorganisms. 4.3. Fish processing industry In the sh processing industry, both equipment and water quality are considered to be major concerns. Also, many types of sh-contaminated-bacteria are found to be biolm-forming, including Vibrio cholerae (Faruque et al., 2006), Vibrio para- haemolyticus (Enos-Berlage, Guvener, Keenan, & McCarter, 2005), Vibrio vulnicus (Joseph and Wright 2004), and Vibrio alginolyticus (Kogure, Ikemoto, & Morisaki, 1998). Many genera other than Vibrio, such as L. monocytogenes, Salmonella spp., Bacillus spp., Aeromonas, and Pseudomonas spp., are also known to be biolm forming in sh and seafood processing (Rajkowski, 2009). As important as any of the other components used in seafood industry, seawater is used instead of freshwater for economical reason. Even though the water is treated in a combined chlorina- tion and Ultraviolet (UV) radiation system, treated seawater was found to be contaminated with Vibrio spp., caused by biolm formation in the seawater distribution system after the treatment process (Shikongo-Nambabi, Kachigunda, & Venter, 2010). Various authors have stated that the failure of chlorine to inhibit biolm formation and mature biolm was not due to the effect of pH (Momba & Binda, 2002; Shikongo-Nambabi et al., 2010). It has been established that there is a loss in water quality after undergoing treatment process, which is usually caused by cells detaching from the biolm in the distribution system due to the ineffectiveness of residual chlorine, and that this is common in water distribution systems (Momba & Makala, 2004; September, Els, Venter, & Brzel, 2007; Shikongo-Nambabi et al., 2010). Furthermore, biolm formation by seafood contaminated Vibrio harveyi on surfacesdbe it plastic, cement slab or steel coupondwas also evaluated. Results showed that there was only a slight reduction of biolm on the concrete slabs and plastic (chlorine 20 ppm; 10 min), while the cells S. Srey et al. / Food Control 31 (2013) 572e585 576 were completely killed at a higher concentration (chlorine 100 ppm; 10 min) on the steel coupons. This is particularly important for shrimp hatcheries given that water storage tanks, polythene water pipes, and surfaces of larval tanks are susceptible to biolm formation (Karunasagar, Otta, & Karunasagar, 1996). In a study by Gubjrnsdttir et al. (2005), it was shown that adhered bacteria are found in many locations on the seafood pro- cessing lines, despite the fact that thorough cleaning and disin- fection are carried out regularly. Gram-negative rods, namely Pseudomonas spp., Aeromonas spp., Enterobacteriaceae, and yeast, were isolated from a shrimp processing plant, while Pseudomonas spp. and Enterobacteriaceae were found mainly in the sh pro- cessing plant. Pseudomonas putida and Pseudomonas uorescens were the main species of Pseudomonas spp. isolated from the shrimp factories. These organisms are considered as the causes of spoilage in fresh or chilled sh (Gram and Huss 1996). More importantly, it was noted that the presence of Pseudomonas spp. would signicantly enhance the colonization of L. monocytogenes on stainless steel (Gubjrnsdttir et al., 2005). It was seen that Vibrio spp. are not the only genus found in seafood processing plants. Other genera such as Pseudomonas spp., Aeromonas spp., and so on are also found to be signicant biolm producers and their presence would enhance the biolm formation of other genus. In another study on the correlation of the biolm forming abilities of Salmonella and its persistence in sh meal- and feed factories, Salmonella agona and Salmonella montevideo were found to be good biolm producers, while Salmonella typhimurium was found to be a poor biolm producer. The results of the study also indicated that the persistence of Salmonella in the factory environment depends signicantly on the strains biolm forming ability (Vestby, Mretr, Langsrud, Heir, & Nesse, 2009). However, it also indi- cated that the level of biolm formation can be affected positively or negatively by environmental factors, such as natural microora (Carpentier & Chassaing, 2004; Gubjrnsdttir et al., 2005). 4.4. Poultry industry Many studies have been carried out on the biolm formation in the poultry processing industry. Under many investigations, it has been identied that dust, surfaces, feces, poultry feed, and trans- portation of live poultry between production and processing units are known to be the important risk factors in Salmonella contami- nation (Marin, Hernandiz, & Lainez, 2009; Park, Jarquin, Hanning, Almeida, & Ricke, 2011; Ramesh, Joseph, Carr, Douglass, & Wheaton, 2002). Furthermore, approximately 50% of the strains isolated on poultry farms were able to produce biolms (Marin et al., 2009). The attachment of 25 Salmonella strains to four different materials (polytetrauoroethylene-also known as Teon, stainless steel, rubber, and polyurethane), which are commonly used in poultry industry, was studied. Among those, Salmonella soa isolates (except S1635 and S1636) can generally adhere in higher numbers to the different surfaces than the other isolates. It was suggested that S. Soa serovar may have more pili or mbriae than others (Chia et al., 2009). The results of the study also agree with the data from Helke et al. (1993) that S. typhimurium can attach more readily to stainless steel than rubber. In a different study, the characterization of biolmformation and the attachment of S. typhimuriumDT104 (Kim& Wei, 2009) was evaluated, with the results indicating that the main contributor to lipopolysaccharide (LPS) synthesis and biolm formation of S. typhimurium DT104 is rfbA gene. According to the study, many factors, such as production of EPS and their efcient transportation through outer membranes, expression of agella and regulation of exoribonucleases and RNA- binding protein, were suggested to be involved in biolmformation and the attachment of S. typhimurium DT104 on contact surfaces. Besides Salmonella spp., Campylobacter spp. are also commonly found pathogens in poultry and poultry processing (Deming et al., 1987; Harris, Weiss, & Nolan, 1986; Hopkins & Scott, 1983; Sanders, Boothe, Frank, & Arnold, 2007). Many researchers have been trying to understand the behavior of Campylobacter jejuni in poultry processing. As a result, it has been determined that temperature is a signicant factor inuencing their survival (Chan, Tran, Kanenaka, & Kathariou, 2001; Dykes et al., 2003; Trachoo, Frank, & Stern, 2002). Other authors have stated that wild-type cultures of C. jejuni planktonic survive longer at lower tempera- tures than higher temperatures when faced with multiple stressors (Chan et al., 2001; Dykes et al., 2003). In contrast, Hanning, Jarquin, and Slavik (2008) showed that culturable C. jejuni can endure longer in biolms at 32
C, compared with survival of culturable planktonic cells and biolms at 10
C. The results of the same study demonstrated that the attachment of C. jejuni to surfaces is facili- tated by a pre-existing biolm so it is important to strengthen the control of biolms in poultry processing. 4.5. Meat industry Organic residues in food processing could be a niche for micro- organism accumulation and biolm formation as it is a source of cross-contamination, and has become quite a concern for numerous researchers (Brooks & Flint, 2008; McLandsborough, Rodriguez, Prez-Conesa, & Weiss, 2006; Simes, Simes, & Vieira, 2010). Many studies have been conducted in order to gain a deeper understanding of biolms. For example, E. coli has been studied by many researchers to investigate the attachment and biolm formation by E. coli O157:H7 at different temperatures, on various food-contact surfaces encountered in beef processing (Dourou et al., 2011). In the results from the study, the cells attached to the surface increased over time even under low temperatures, which could result from the migration of cells toward the surface by agellar-mediated motility and Brownian motion (Van Houdt & Michiels, 2005). It has been seen that at low temperatures, micro- organisms can adhere and survive on food contact surfaces, and even increase in population as time progressed (Dourou et al., 2011; Kim, Ryu, & Beuchat, 2006). Another important factor inuencing the attachment of E. coli O157:H7 is the presence of other micro- organisms on the surfaces (Castonguay et al., 2006; Klayman, Volden, Stewart, & Camper, 2009; Marouani-Gadri, Augier, & Carpentier, 2009). As an example, E. coli O157:H7 was found to be incapable of forming a biolm under dynamic-ow conditions due to the shear forces, while Acinetobacter calcoaceticusdisolated from meat-processing plantsdmonospecies biolms are heterogeneous, well organized, and can develop under both static and dynamic conditions. The research of Habimana, Heir, Langsrud, Asli, and Mretr (2010) indicated that E. coli O157:H7 cells were embedded and cover by a Acinetobacter calcoaceticus biolm under both static and dynamic growth conditions. It is now well docu- mented that multispecies biolms may increase the opportunities for pathogens to thrive in the food industry (Burmlle et al., 2006; Habimana et al., 2010; Stewart & Franklin, 2008). 4.6. Ready-to-eat (RTE) foods industry Due to lifestyle changes, RTE foods have become very popular. However, RTE foods can be considered as a relatively high risk food since the products will be consumed directly without undergoing any bactericidal process. Even though RTE foods have been well processed, the chances of being contaminated are relatively high. Furthermore, the storage times and conditions are known to be important factors affecting RTE foods quality (Sofos & Geornaras, 2010). RTE foods could potentially be susceptible to cross- S. Srey et al. / Food Control 31 (2013) 572e585 577 contamination during processing and handling. In particular, after cooking, the products may be recontaminated during loading, conveying, weighing, and packaging (Osaili, Alaboudi, & Nesiar, 2011). Garrido et al. (2009) evaluated the occurrence and levels of L. monocytogenes in refrigerated RTE products for prolonged consumption in northern Spain. It was found that RTE smoked sh was the most common pathogen-contaminated food among the samples analyzed. The slicing materials used in processing were speculated to be the source of contamination due to biolm formation. Comparably, smoked salmon was found to be the most L. monocytogenes contaminated product in the study by Di Pinto, Novello, Montemurro, Bonerba, and Tantillo (2010). According to a survey by Wagner, Auer, Trittremmel, Hein, and Schoder (2007), sh and seafood were also found to be highly contaminated with L. monocytogenes among the samples analyzed. The survey also shows that there is more chance of contamination for unpackaged or repackaged RTE foods; furthermore, raw meat sausages were postulated to be potentially contaminated. In addition, the production of biolms and quorum sensing by E. coli O157:H7 and its transfer from contact surfaces to meat, poultry, RTE deli prod- ucts, and produce products was studied. As a result, the E. coli O157:H7 strain could be a concern in a wide variety of food prod- ucts since it can form biolms on food contact surfaces during food processing (Silagyi, Kim, Lo, & Wei, 2009). 5. Biolm control strategies Since biolms are a great concern in the food sectors, many studies have been done in order to gain a better understanding of their development and spread. Consequently, many studies have also come up with countermeasures. The rst and most important thing to do is to prevent biolm formation by regularly cleaning and disinfecting so as to not allow the cells to rmly attach (reversible attachment) to contact surfaces (Midelet & Carpentier, 2004; Simes, Simes, Machado, Pereira, & Vieira, 2006). Meyer (2003) suggested three different strategies: (i) disinfection in time, before biolm develops, (ii) disinfection of biolms using harsh disinfectants, and (iii) inhibition of attachment of microbes by selecting surface materials that do not promote attachment or by supplementing with nutrients. Many other researchers have accounted for the incorporation of antimicrobial products in the surface materials themselves (Knetsch & Koole, 2011; Park, Daeschel, & Zhao, 2004) by coating surfaces with antimicrobials (Knetsch & Koole, 2011; Thouvenin et al., 2003) or by modifying the surfaces physiochemical properties (Chandra et al., 2005; Rosmaninho et al., 2007). In a study on biolm control, micropar- ticles (CaCO 3 ) coated with benzyldimethyldodecylammonium chloride were found to effectively inactivate biolm formation (Ferreira, Pereira, & Pereira, 2011). Many others reported biolm formation was inhibited by silver coating surfaces (Hashimoto, 2001; Knetsch & Koole, 2011). Pre-conditioning the surface with a surfactant has also been reported to prevent bacterial adhesion (Chen, 2012; Choi, Park, Lee, Park, & Kim, 2011). The research of Zeraik and Nitschke (2010) demonstrated that after conditioning with surfactant, the surface became more hydrophilic. The data illustrated the decrease in hydrophobicity on the treated surfaces and showed a signicant decrease in bacterial attachment. However, other factors are still considered to contribute to the reduction of bacterial attachment. 5.1. Cleaning and disinfection In the food industry, there is debris everywhere which would promote the accumulation of microorganisms and encourage bio- lm formation. Therefore, regular cleaning is required so as to prevent the contamination of food products. A good cleaning process that removes any food residues and other compounds that may promote bacteria proliferation and biolm formation is particularly effective (Simes et al. 2010). Many different chemical products may be used in cleaning, including surfactants or alkali products, or used to suspend and dissolve food debris by decreasing surface tension, emulsifying fats, and denaturing proteins (Forsythe & Hayes, 1998; Maukonen et al., 2003). Cleaning should be carried out in a way that can break-up or dissolve the EPS matrix associated with the biolms so that disinfectants can gain access to the bacteria cells (Simes et al. 2006). It is evident that the use of high temperatures in cleaning can reduce the physical force required, such as water turbulence and scrubbing (Maukonen et al., 2003); as well as inactivate biolm cells at a certain level (Chmielewski & Frank, 2006). Besides, cleaning only allows the removal of approximately 90% of the bacteria from the surfaces and does not kill them. They might later re-attach to other surfaces and form a biolm, thus disinfection is indispensible with the intention of eliminating them(Gram, Bagge-Ravn, Ng, Gymoese, & Vogel, 2007). Antimicrobial agents are used in the disinfection process so as to kill microorganisms so that the surface population is reduced along with microbial growth on the surfaces. However, the effectiveness of disinfectants is limited by the presence of organic material including fat, carbohydrates, and protein-based materials. Other than that, pH, temperature, water hardness, chemical inhibitors, concentration, and contact time are also important factors inu- encing disinfectants effectiveness (Bremer, Monk, & Butler, 2002; Cloete, Jacobs, & Brzel, 1998; Kuda, Yano, & Kuda, 2008). There are many types of disinfectants including chlorine, hydrogen peroxide, iodine, ozone, peracetic acid (Chmielewski & Frank, 2007). 5.2. Clean-in-Place (CIP) Clean-in-Place (CIP) is a process allowing a complete system to be cleaned without dismantling it or the manual involvement of the operator. It includes jetting and spraying the surfaces or the circulation of cleaning solutions throughout the plant with an increased turbulence and ow velocity (Romney, 1990). There are many factors that can inuence CIP efcacy, including the nature of the biolm layer, cleaning chemical composition and concen- tration, time (Boulange-Petermann, Jullien, Dubois, Benezech, & Faille, 2004; Changani, Belmar-Beiny, & Fryer, 1997), cleaning temperature (Lelivre, Faile, & Bnzech, 2001), cleaning ow rate and hydrodynamic (Lelivre, Antonini, Faille, & Bnzech, 2002), and the cleaning surface characteristics (Lelivre, Legentilhomme, et al., 2002). Relatively, Walton (2008) also summarized the basic principles of cleaning to (i) consider the physical nature and construction of the equipment to be cleaned, (ii) assess the nature of the soil to be removed; (iii) select a detergent appropriate to the removal of that soil, (iv) bring the soil and the detergent together (at the right temperature, under the right conditions of ow and turbulence, at the right chemical concentration, for the right period of time), (v) rinse away all traces of detergent and soil, with the objective of achieving the standard of cleanliness appropriate to the duty for which the equipment is destined to be used, (vi) always undertake cleaning as soon as possible after completion of the production operation, and (vii) when necessary, undertake a disinfection or sterilization process immediately before the equipment is returned to processing or production duties in order to reduce the level of microbiological contamina- tion to one consistent with the hygienic standard required for that duty. Bremer, Fillery, and McQuillan (2006) mimicked the CIP of dairy biolms on a laboratory scale to study the effectiveness of the different caustic and acid wash steps. According to the results, it S. Srey et al. / Food Control 31 (2013) 572e585 578 was postulated that the efcacy of the cleaning conditions con- ducted may change according to the amount of soiling and cleaning cycles, as well as the fact that the removal of bacterial biolms on surfaces in a dairy manufacturing plant can be improved by using caustic and nitric additives. In another study, the life cycle of four CIP methods (conventional alkaline/acid cleaning with hot water disinfection, one-phase alkaline cleaning with acid chemical disinfection, enzyme-base cleaning with acid chemical disinfection and the conventional method with disinfection by cold nitric acid at pH 2) was evaluated. It was found that the CIP methods with small volumes and low temperatures, such as enzyme-based cleaning and one-phase alkaline cleaning, were the most highly recom- mended alternative methods (Eide, Homleid, & Mattsson, 2003). The study on biolm removal of bacterial isolates sampled in the food industry by enzymes proposed that the implementation of enzymatic control of bacterial biolms in the food industry would present a noteworthy alternative, while the conventional CIP using chemical agents is not providing satisfactory hygienic results (Lequette, Boels, Clarisse, & Faille, 2010). 5.3. Chemical-based control In the study on the effect of mechanical stress on biolms challenged by different chemicals, it was stated that chemical agents would react with the EPS complex which would enhance the mechanical biolm removal. The removal rate was signicantly improved after treating the biolm with chemical agents (Simes, Pereira, & Vieira, 2005). However, in another study, bacterial cells were destroyed after being subjected to chemical agents, while the EPS matrix was left unaffected. The best result was attained by applying both chemical and mechanical treatment (Exner, Tuschewitzki, & Scharnagel, 1987). Accordingly, it was suggested that mechanical treatment cannot remove bacterial cells (Jessen & Lammert, 2003). As such, it can be postulated that chemical and mechanical treatment has a synergistic effect and both play important roles in biolm and bacterial cell removal. 5.3.1. Sodium hypochlorite Sodium Hypochlorite (NaClO) is a chemical compound used for bleaching or disinfection and as such it has been used for dis- infecting surfaces. It was reported to be an effective disinfectant for biolm inactivation (Ozdemir, Buzoglu, Calt, Stabholz, & Steinberg, 2010; da Silva et al., 2011). However, it is known to be more effective in low pH than alkaline pH environments (Arajo, Lemos, Mergulho, Melo, & Simes, 2011). NaClO was reported to be a potential biolm antimicrobial agent against Staphylococcus aureus (Tot, Horemans, Vanden Berghe, Maes, & Cos, 2010), Prevotella intermedia, Peptostreptococcus miros, Streptococcus inter- medius, Fusobacterium nucleatum, and Enterococcus faecalis when compared to other disinfectants used in a study by Spratt, Pratten, Wilson, and Gulabivala (2001). In a study by Lomander, Schreuders, Russek-Cohen, and Ali (2004), 50 ppm sodium hypochlorite solu- tion was able to signicantly eliminate biolm cells compared to rinsing in water. In the comparison on detaching biolmremoval, it was not more effective than water in detaching biolms. Six percent NaClO was also reported to be able to kill a signicant amount of E. faecalis biolms, which is statistically better than other tested agents. The efciency of NaClO was tested in the elimination of L. monocytogenes, Pseudomonas fragi and Staphylococcus xylosus (Norwood & Gilmour, 2000). Consequently, all planktonic cells were eliminated with an exposure to 10 ppm free chlorine for 30 s, while it can reduce only 2 log of a L. monocytogenes biolm with a concentration of 1000 ppm with an exposure time of 20 min. It was speculated that the co-cultured biolm may enhance its resistance to disinfectants. 5.3.2. Hydrogen peroxide (H 2 O 2 ) H 2 O 2 is one of the widely used disinfectants due to its highly oxidizing capacity based on the production of free radicals which affect the biolm matrix and has been found to be efcient against biolms (de Carvalho, 2007; de Carvalho & da Fonseca, 2007). Moreover, many studies have shown its efciency as a disinfectant against biolms (Christina, Penna, Mazzola, Maria, & Martins, 2001; Tot et al., 2010). Fromthe perspective of safety, H 2 O 2 is known to be a safe solution which does not cause allergic reactions (Rideout, Teschke, Dimich-Ward, & Kennedy, 2005). Moreover, Kim, Silva, Chamul, and Chen (2000) showed that H 2 O 2 can be used at a high concentration without negatively affecting the product quality. H 2 O 2 was used against four strains of Vibrio spp. in seawater. It was found to be very effective in inhibiting biolm formation at a concentration of 0.05% (500 mg/l). It can also kill mature biolms at concentrations between 0.08% and 0.2% (Shikongo-Nambabi et al., 2010). In this study, the bacteria killing efciency was higher than the previous study of Kim et al. (2000). It is postulated that the different mineral ions present in seawater are essential in the enhancement of H 2 O 2 reaction against microorganism (Shikongo-Nambabi et al., 2010). Likewise, it was reported to completely eradicate biolms at a concentration of 5% with a 15 min exposure time (Robbins, Fisher, Moltz, & Martin, 2005). 5.3.3. Ozone Ozone, a result of oxygen atoms exposed to high-voltage electric discharge, is a bluish gas with strong odor and potential oxidizing properties (Horva
th, Bilitzky, & Httner, 1985, p. 350). It is a potent antimicrobial agent which can be used against bacteria, fungi, viruses, protozoa, and bacterial and fungal spores (Khardre, Yousef, & Kim, 2001). The microorganisms are eradicated by the disruption or breakdown of the cell envelope, which in turn leads to the leakage of the cell contents. Cell lysis is a faster inactivation mechanism than that of other antimicrobial agents where perme- ation through the cell membrane is indispensable in order to effectively inactivate the microbe. Due to its mechanism, it is speculated that it cannot lead to microorganismresistance (Pascual, Llorca, & Canut, 2007). Many researchers have demonstrated the efciency of ozone against bacterial cells and biolms (Dosti, Guzel- Seydim, & Greene, 2005; Lagrange, Reiprich, & Hoffmann, 2004). A study by Tachikawa, Yamanaka, and Nakamuro (2009) on the disinfection and removal of biolms by ozone water on P. uorescens and P. aeruginosa biolms showed that by forming biolms, the resistibility of the microorganisms against ozone was increased by 3000 and 10 times, respectively. The reason behind the resistance could be the reaction between ozone and the biolm matrix introduced into the environment by the bacteria. However, the surviving cells were found to be less than 1% after being treated with ozone. 5.3.4. Peracetic acid Peracetic acid is a result of the reaction between hydrogen peroxide and acetic acid, or by the oxidation of acethaldehyde. The mixture has a strong odor and a low pH (2.8) and is usually produced in concentrations between 5 and 15%. It has been used in water purication and as a disinfectant (Anonymous, n.d.-a). It is known as an ideal antimicrobial agent according to its extreme oxidizing capacity. Furthermore, it cannot be deactivated by cata- lase and peroxidasedenzymes that degrade H 2 O 2 . This agent also decomposes into safe and environmental friendly residues in food (acetic acid and hydrogen peroxide), hence it can be applied without rinsing and its efcacy is not affected by protein residues (Anonymous, n.d.-b). A study showed that peracetic acid can reduce L. monocytogenes biolm adhered for 24 h by 5 log with a concen- tration of 0.50% w/v (Cabea, Pizzolitto, & Pizzolitto, 2008). S. Srey et al. / Food Control 31 (2013) 572e585 579 According to Frank, Ehlers, and Wicker (2003), peracetic acid can reduce more than 6 log of L. monocytogenes biolms on stainless steel in the presence of fat and protein soil with a concentration of 2.0 ml/l and an exposure time of 10 min. Others studies also showed the effectiveness of peracetic acid against various micro- organisms (Marques et al., 2007; Salvia, Teodoro, Balducci, Koga- Ito, & Oliveira, 2011). According to Tot et al. (2010), peracetic acid eliminated approximately 98% and 99% of viable S. aureus and P. aeruginosa, respectively, with only 1 min of contact time but not the biolm matrix. However, there are also several other studies which showed that peracetic acid is inefcient or less effective than other disinfectants against biolms (Krlasik, Zakowska, Krepska, & Klimek, 2010; Rossoni & Gaylarde, 2000). It is suggested that aldehydes do not degrade the biolm matrix, and instead improve the stability. The biolm complex needs to be eradicated before chemical agents can be used effectively (Exner et al., 1987). 5.4. Other approaches of biolm control The conventional control strategies are chemical-based, however, it is possible that microorganisms hold a certain degree of resistance to such strategies, or may acquire it later through mutation or genetic exchange. These processes enable the bacteria to survive and proliferate under higher concentration of disinfec- tants (Gilbert & Mcbain, 2003; McBain, Rickard, & Gilbert, 2002). Therefore, new approaches to controlling biolms in the food industry have been introduced. Simes et al. (2010) reviewed potential green strategies, including control using enzyme, phage, and microbial interactions and metabolite molecules. 5.4.1. Ultrasonication Ultrasonication is a well known technique used in various food industry processes namely freezing, cutting, drying, tempering, bleaching, sterilization, and extraction (Chemat, Zill-e-Huma, & Khan, 2011). It was reported to also be used as an efcient biolm removal method (Oulahal-Lagsir, Martial-Gros, Boistier, Blum, & Bonneau, 2000a). Oulahal-Lagsir, Martial-Gros, Bonneau, et al. (2000b) investigated the use of an ultrasonic apparatus on biolm removal from stainless steel and polypropylene surfaces. The apparatus was demonstrated to be able to remove twice as much of the industrial milk biolm as the swabbing method on poly- propylene sheets. However, it has been documented that even though lower-frequency in sonation is remarkably more efcient than higher frequency for reducing biolm cells viability, bacteria in food industries cannot be solely eliminated using the present ultrasonic technologies thus combining techniques of ultrasound with other treatment techniques were recommended (Piyasena, Mohareb, & McKellar, 2003; Qian, Sagers, & Piti, 1997). Accord- ingly, the combination of ultrasound and ethylenediaminetetra- acetic acid (EDTA), and ultrasound and enzymes showed a higher efcacy in removing biolms. The results were more promising against S. aureus than E. coli biolms in the study. The authors stated that this method was in agreement with an industrial control method, i.e. a combined treatment of ultrasound generation in enzymes preparation restricted to an active chamber area with a fast and good reproducible recovery compared to other approaches (Oulahal, Martial-Gros, Bonneau, & Blum, 2007). Ultrasound was also reported to increase the effectiveness of antibiotics against biolm cells (Peterson & Pitt, 2000). Two processes were observed to be account for the increased efciency: i), ultrasound improves the diffusion of oxygen into the biolm matrix which allows biolm cells to become active, and therefore, affected by antibiotics and ii), the high ratedenhanced by ultrasounddof antibiotics transported into the complex may destroy the bacteria before they gain resistance to the agents (Carmen et al., 2004). Baumann, Martin, and Feng (2009) also showed a signicant effect on biolm removal on stainless steel food contact surfaces by combining the use of ozonation and sonication. 5.4.2. Enzymes Enzymes are proteins with catalytic activity on a specic chemical molecule. It can be an important alternative for biolm removal in the food industry. However, EPS is a heterogenic matrix so, in order to degrade the complex, a combination of enzymes is required (Simes et al. 2010). Lequette et al. (2010) showed that the enzymes efciency on biolm removal may vary according to the species of bacteria and it can also be enhanced by combining with surfactants; this suggests that proteins also contribute to the adhesion of biolms as proposed by Hinsa and OToole (2006). The research of Molobela, Cloete, and Beukes (2010) indicated that protease enzymes were effective in the degradation of P. uorescens biolms EPS, while amylase enzymes were less effective. It was suggested that the structural composition of EPS varies even among bacteria of the same species, with the way they were formulated and their mode of action, are the reasons for the enzymes inef- ciency. It is well known that a mixture of proteases and amylases is commonly used to respond to the variety present in a single biolm. While proteases hydrolyze the proteins, amylases break the bond of carbohydrates associated with the complex. Among all 1,4-glycosidic bond cleaving amylases, a-Amylases are frequently used because of their thermostability; however, they will not stay active for long as they are calcium metalloenzymes (Craigen, Dashiff, & Kadouri, 2011). Similarly, a combination of polysaccharide-hydrolyzing enzymes and oxidoreductases were recommended for bacteria biolmremoval due to the wide range of polysaccharide-hydrolyzing enzymes activities which make it useful for the degradation of biolms matrix; the bactericidal effect of oxidoreductases (Johansen, Falholt, & Gram, 1997). In another study, individual biolm cleaning efciencies of pectin esterase, pectin lyase, and cellulose were shown to be not as effective against P. uorescens mature biolms. However, the efcacy was enhanced when pronase was used in the treatment process, and after being treated with the aforementioned enzymes and the detachment- promoting-agent, pronase, to simultaneously treat with others enzymes (Orgaz, Neufeld, & Sanjose, 2007). As can be seen, enzy- matic control against biolms could be used as a newand improved environmental friendly alternative strategy according to its nontoxic characteristics and instability. 5.4.3. Phages The rst application of phages was in the early 20th century for bacterial infections treatment in Eastern Europe, and have been shown to decrease biolm formation (Curtin & Donlan, 2006; Merril, Scholl, & Adhya, 2003). Unlike chemical-based antimicrobial agents that can cause corrosion, phages can be a suitable substitute (Goldman, Starosvetsky, & Armon, 2009), thus it has also been proposed as a biolm control method (Curtin & Donlan, 2006). Bacteriophage spray treatment was suggested to be an alternative to dipping, brushing, or sponging of the spinach harvester blade on a chlorine solution according to its compatibility with harvest sanitation practices (Patel, Sharma, Millner, Calaway, & Singh, 2011). It was documented that phage components and their assembly synthesis vary according to the host bacterial growth rate and their amount of protein-synthesizing during the time of infection; however, it was also reported that even under a glucose- limited chemostat, T4 phage can effect E. coli biolms (Corbin, McLean, & Aron, 2001). In a study on the effect of the phage philBB-PF7A on P. uorescens biolms, the important role of convection mechanism was discussed. It was said that biolm cells S. Srey et al. / Food Control 31 (2013) 572e585 580 lysis is more efcient under static conditions than dynamic conditions. It was also found that fIBB-PF7A could be a remarkable biological agent according to its biolm cells lysing capability in a markedly rapid time (Sillankorva, Neubauer, & Azeredo, 2008). The same phage was also used to control the dual species biolm of P. uorescens and Staphylococcus lentus, and accounted for the dramatic decrease in the target bacteria cells (P. uorescens). Surprisingly, it was proved that phages can be used to efciently reach and lyse their target bacterium in both single and dual species biolms notwithstanding the presence of a non-susceptible host (Sillankorva, Neubauer, & Azeredo, 2010). Cerca, Oliveira, and Azeredo (2007) studied the susceptibility of S. epidermidis planktonic cells and biolms according to the lytic action of staphylococcus bacteriophage K. The phage K lysis ef- ciency depends upon the bacteria growth phase. This was also found to be true in the research of Sillankorva, Oliveira, Vieira, Sutherland, and Azeredo (2004). Fluorescence Correlation Spec- troscopy was used to study the diffusion and reaction of bacterio- phages inside biolms; the results indicated that bacteriophages can inltrate different biolm complexes, and that generally, they are immobilized, amplied, and released by a lytic cycle in the biolm and interact with their specic binding sites on the hosts although the lytic activity was not observed (Briandet et al., 2008). According to Tait, Skillman, and Sutherland (2002), phages and bacteria can steadily co-exist in biolms, thus a mixture of phages and polysaccharide depolymerases and disinfectant was suggested for a better biolm control. To address this challenge, bacterio- phages can be engineered to be able to express a biolm-degrading enzyme, which would be a good asset in overcoming the challenges in controlling biolms. The engineered phages were reported to be able to noticeably eradicate bacterial cells in biolms (approxi- mately 99.997% removal), as well as the biolm complex (Lu & Collins, 2007). 5.5. Hurdle technology Hurdle technology is a combination of two or more different control techniques which have been proven to be effective. However, in order to achieve an effective treatment, the right combination is needed. It was shown that the combination treat- ment of NaClO with UV irradiation had a better reduction of food- borne pathogens in food than single treatment (Ha & Ha, 2011). DeQueiroz and Day (2007) studied the antimicrobial activity and effectiveness of a combination of NaClO and hydrogen peroxide (H 2 O 2 ) in killing and removing P. aeruginosa biolms from surfaces. It showed an increased reduction in the number of cells with only a short exposure time. The synergistic effect of a combined treat- ment of biolms with H 2 O 2 and UV was also shown to be more effective than the single use of H 2 O 2 by 10 fold, which could contribute to a more environmental-friendly treatment (Vankerckhoven et al., 2011). Schurman, Sumner, and Marcy (2001) tested the effectiveness of H 2 O 2 and demonstrated that its efcacy was enhanced when there was an increase in temperature. More- over, an increase in organic acid concentration could also increase its efciency. Additionally, the synergistic effect of ozone and ultrasound was also shown to be efcient for biolm cell reduction. However, the amount of cells eradicated was only slightly more compared to that when ozone was used alone. It was suggested that the energy efciency of the combined process shall be studied in order to have a cost-effective treatment system (Patil, 2010). Moreover, the efciency of antibiotics alone and synergizing with a lytic bacteriophage in the removal of old Klebsiella pneumoniae biolms was examined. The ndings revealed that phages can be surprisingly capable in the removal of older biolms on account of depolymerase. Thenagain, the eradicationof biolms was improved when a bacteriophage is used with an antibiotic (Verma, Harjai, & Chhibber, 2010). Hurdle technology is a very promising new approach in controlling biolms in the food industry. 6. Conclusion Pathogenic microorganisms in biolms formed in different food industries settings are a source of food contamination. As the demand for fresh, RTE and processed foods increases, many studies are needed to address biolm removal and disinfectant efcacy in food industries. 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