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Mini Review ARTICLE
Potential Impact of the Resistance to Quaternary Ammonium Disinfectants on the Persistence of Listeria monocytogenes in Food Processing Environments
- 1Departamento de Tecnología de Alimentos, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Madrid, Spain
- 2Unidad de Biología Computacional, Unidad Funcional de Investigación de Enfermedades Crónicas, Instituto de Salud Carlos III, Madrid, Spain
The persistence of certain strains of Listeria monocytogenes, even after the food processing environment has been cleaned and disinfected, suggests that this may be related to phenomena that reduce the concentration of the disinfectants to subinhibitory levels. This includes (i) the existence of environmental niches or reservoirs that are difficult for disinfectants to reach, (ii) microorganisms that form biofilms and create microenvironments in which adequate concentrations of disinfectants cannot be attained, and (iii) the acquisition of resistance mechanisms in L. monocytogenes, including those that lead to a reduction in the intracellular concentration of the disinfectants. The only available data with regard to the resistance of L. monocytogenes to disinfectants applied in food production environments refer to genotypic resistance to quaternary ammonium compounds (QACs). Although there are several well-characterized efflux pumps that confer resistance to QACs, it is a low-level resistance that does not generate resistance to QACs at the concentrations applied in the food industry. However, dilution in the environment and biodegradation result in QAC concentration gradients. As a result, the microorganisms are frequently exposed to subinhibitory concentrations of QACs. Therefore, the low-level resistance to QACs in L. monocytogenes may contribute to its environmental adaptation and persistence. In fact, in certain cases, the relationship between low-level resistance and the environmental persistence of L. monocytogenes in different food production chains has been previously established. The resistant strains would have survival advantages in these environments over sensitive strains, such as the ability to form biofilms in the presence of increased biocide concentrations.
Listeria monocytogenes is a Gram-positive foodborne pathogen that can cause listeriosis, a relatively uncommon illness with a 20–30% case fatality rate (Silk et al., 2012; CDC, 2014; de Noordhout et al., 2014; EFSA and ECDC, 2014). The majority of cases of human listeriosis are caused by contaminated processed foods (McLauchlin et al., 2004; Lianou and Sofos, 2007). Although the original source of the contamination may be the raw food materials used in the processing plants, the strains of L. monocytogenes present in the final food products are usually different from the strains in the raw materials (Tompkin, 2002; Thévenot et al., 2006). In addition, when listeriosis outbreaks have been investigated, contamination is usually traced to the processing environment and equipment (Orsi et al., 2008; Nakari et al., 2014). This suggests that the contamination mainly occurs during the processing of food and is primarily due to strains from the processing plant environment (Malley et al., 2015; Garner and Kathariou, 2016).
Environmental Persistence
The molecular characterization of L. monocytogenes isolates from the food processing environment regularly shows the presence of a reduced number of molecular subtypes and the long-term persistence of specific strains that can contaminate food and cause foodborne listeriosis (Ortiz et al., 2010; Ferreira et al., 2011; Morganti et al., 2015). The detection of highly similar isolates from different areas inside single establishments, and their environmental persistence, is a matter of concern for the hygienic management of food establishments (Cramer, 2006; Ferreira et al., 2014).
Carpentier and Cerf (2011) assert that L. monocytogenes persistence is primarily a random process given that "there are no strains with unique properties that lead to persistence but harborage sites in food industry premises and equipment where L. monocytogenes can persist." Persistent strains of L. monocytogenes have occasionally been isolated in food processing environments after cleaning and disinfection (Lundén et al., 2003b; Soumet et al., 2005; Thévenot et al., 2006; Bērziņš et al., 2010; Ortiz et al., 2016). As demonstrated by the findings of studies reviewed here, the persistence of certain strains of L. monocytogenes after cleaning and disinfecting is not a completely random process, but rather an event related to different situations that result in subinhibitory concentrations of disinfectants at different scales. This includes: (i) local environmental conditions that can lead to the formation of niches or reservoirs that are difficult for disinfectants to reach; (ii) microorganisms that form biofilms and create microenvironments in which adequate concentrations of disinfectants cannot be attained; and (iii) the acquisition of resistance mechanisms in L. monocytogenes, including those that lead to a reduction in the intracellular concentration of the disinfectants.
There are numerous factors in food processing plants, such as insufficient cleaning before disinfection, disinfection of wet surfaces, and dosage failure that can lead to subinhibitory concentrations of disinfectants, thus reducing their efficiency. This reduction may be especially significant in certain niches or reservoirs in which water and organic matter are abundant, creating an environment where bacteria can survive and multiply readily (Cramer, 2006; Carpentier and Cerf, 2011).
Failure to effectively clean and disinfect the processing plant environment may contribute to biofilm formation in certain niches, leading to bacterial persistence (Gandhi and Chikindas, 2007; Renier et al., 2011). Cells embedded in the biofilm matrix display an increased resistance to biocide treatments (Bridier et al., 2011). However, the resistance to disinfectants in sessile cells (biofilms) and in planktonic cells (free-floating) are clearly different phenomena (Fatemi and Frank, 1999; Norwood and Gilmour, 2000; Stopforth et al., 2002; Kastbjerg and Gram, 2009). Resistance of biofilms to disinfectants is considered to be a form of "phenotypic resistance" since bacterial resistance is mainly induced by a physiological adaptation to the biofilm mode of life and can be lost or markedly reduced when biofilm cells revert to the planktonic state (Pan et al., 2006; Bridier et al., 2011). In contrast, in the case of planktonic cells, a bacterial strain is defined as being resistant to a biocide if it is not inhibited by a specific concentration that usually inhibit the majority of other strains (Bridier et al., 2011); that is, planktonic cell resistance depends on intrinsic cellular attributes such as intra-species (i.e., strain) variability in the MIC of a given disinfectant (Kastbjerg and Gram, 2012).
Resistance to Disinfectants
The only available data with regard to the resistance of L. monocytogenes to disinfectants applied in food production environments refer to genotypic resistance to QACs (Hegstad et al., 2010; Gerba, 2015). BAC is typically used in studies assessing in vitro the activity of QACs. Increased MICs of BAC have been found in L. monocytogenes strains from different food production chains in different countries (Table 1). BAC resistance in L. monocytogenes is a low-level resistance. This means that the resistant strains only have a two to eight-fold increase in the MIC compared to the rest of the strains (Table 1). This resistance does not lead to QAC resistance at the concentrations that are normally used in the food industry (typically 200–1000 mg L-1) (SCENIHR, 2009; Ferreira et al., 2014; Tezel and Pavlostathis, 2015). Therefore, QACs are considered to be an effective means of eliminating the resistant L. monocytogenes strains (Kastbjerg and Gram, 2009, 2012).
Some of these studies have been conducted with a large number of strains, and they report a variable frequency of resistant strains due to the diversity of the selection criteria for the strains studied. For example, the study of Ortiz et al. (2016) reports a very high frequency of resistant isolates because only samples of disinfected surfaces are included (Table 1). In some cases, selection for L. monocytogenes isolates resistant to QACs has been associated with the repeated use of this class of disinfectants (Heir et al., 2004; Ortiz et al., 2014a, 2016).
In food processing environments, L. monocytogenes is exposed to different disinfectants and sanitizers, and sometimes at subinhibitory cocentrations. This is particularly true for disinfectants that are not fully biodegradable which may persist in sewage for long periods. For example, QACs are biodegradable only under aerobic conditions, resulting in continuously fluctuating concentration gradients (Tezel and Pavlostathis, 2015). As a result, the microorganisms are frequently exposed to subinhibitory concentrations of QACs. Repeated exposure to subinhibitory concentrations of QACs and prolonged environmental persistence of certain strains may facilitate the development of resistance over time (Ortiz et al., 2014a). Subinhibitory concentrations of antimicrobials may cause genetic changes in the bacteria by means of different pathways, including an increase in free radicals inside the cell or oxidative stress (Liu et al., 2016). This can trigger the SOS response which can promote either the expression of genes involved in horizontal gene transfer or mutagenesis through induction of the error-prone DNA polymerases (Shapiro, 2015).
Strains of L. monocytogenes with genotypic resistance to QACs may have mutations that lead to a reduction in cell permeability (Mereghetti et al., 2000; To et al., 2002). For instance, resistant strains may have modifications in membrane fatty acids and phospholipids (Fox et al., 2011), which can lead to a more anionic and hydrophobic cell surface. This makes it difficult for QACs to pass through the membrane and enter the cell (To et al., 2002).
In other cases, resistance to QACs in L. monocytogenes may be due to the acquisition of QAC-specific efflux pumps through recombinant elements and mobile genetic elements. Different genetic markers have been identified that confer L. monocytogenes with a low-level resistance to QACs, including the resistance determinant bcrABC (Elhanafi et al., 2010) and the qacH gene of transposon Tn6188 (Müller et al., 2013), as well as various qac determinants originally identified in staphylococci (Xu et al., 2014). All of these genes encode components of the efflux system in the small multidrug resistance (SMR) protein family group (Blair et al., 2015). Plasmids are also associated with L. monocytogenes resistance to BAC (Elhanafi et al., 2010). Furthermore, plasmids with genes that confer resistance to BAC can be transferred between different pathogenic and non-pathogenic species of Listeria in the presence of QACs. This process also leads to the co-selection of resistance against heavy metals (Katharios-Lanwermeyer et al., 2012). In several screening studies of resistant strains, the qacH gene and the determinant bcrABC have been found (Müller et al., 2013). In one study, for example, resistance to BAC has been associated with the qacH gene in the majority (80%) of the tested strains, and a minority of the strains (12%) have been associated with the determinant bcrABC (Ebner et al., 2015). Nevertheless, in other studies, only the qacH gene has been detected (Ortiz et al., 2014b, 2016), while in others a clear predominance of the determinant bcrABC has been reported (Dutta et al., 2013).
On the other hand, in some studies, the aforementioned determinants are not detected in certain resistant strains (Ortiz et al., 2014b, 2016; Ebner et al., 2015). In these cases, resistance may be due to the overexpression of endogenous efflux pumps due to mutations in regulatory elements. This can occur due to exposure to QACs or the stress induced by these compounds (Tezel and Pavlostathis, 2015). These pumps are usually chromosomally encoded and affect a broad spectrum of antimicrobial compounds (Buffet-Bataillon et al., 2012; Ortiz et al., 2016). In certain strains of L. monocytogenes that are resistant to BAC, QAC resistance has been associated with the overexpression of efflux pumps in the MFS (major facilitator superfamily) group (Blair et al., 2015), such as MdrL (multidrug resistant Listeria) and Lde (Listeria drug efflux) (Romanova et al., 2006; Rakic-Martinez et al., 2011). Recently, the overexpression of a new L. monocytogenes efflux pump (encoded by emrE) has been implicated in the resistance to QACs (Kovacevic et al., 2015).
The Problem of Defining and Detecting Resistance
For various reasons, data on bacterial resistance to biocides is often difficult to interpret and compare (Buffet-Bataillon et al., 2012). A potential reason for the difficulty in interpreting data on bacterial resistance to biocides is the absence of clear criteria for defining a microorganism as resistant to disinfectants. An ecological concept of resistance to biocides has been proposed based on the "natural" susceptibility of a given species (Morrissey et al., 2014). According to this criterion, an isolate is defined as resistant when it is not inhibited by a concentration that would inhibit most of the strains of that particular species. The resistant isolate is typically phenotypically different from the wild type because it has acquired a resistance mechanism through mutation or horizontal gene transfer (EFSA, 2008; SCENIHR, 2009; Buffet-Bataillon et al., 2012; Morrissey et al., 2014). This commonly happens to L. monocytogenes strains that are resistant to BAC (Mereghetti et al., 2000; Elhanafi et al., 2010; Müller et al., 2013).
Another reason for the difficulty in comparing results on bacterial resistance is the lack of standardized tests for examining in vitro susceptibility to disinfectants (Buffet-Bataillon et al., 2012). Susceptibility to disinfectants is often determined through the MIC technique (usually employing agar dilution or broth dilution methods) (Table 1). However, in some cases, the MICs obtained through different methods can produce different results, which is why standardization is necessary. The influence of the culture media is especially important to consider when detecting low-level resistance (Table 1). Therefore, we recommend the use of standardized clinical protocols that are designed to evaluate the inhibitory activity of antibiotics (EUCAST, 2000; CLSI, 2009). Consequently, changes in the MIC of the disinfectant of several "test" strains can be measured and the resistant strains can be detected (Ortiz et al., 2014a). In contrast, current standardized tests for the evaluation and comparison of commercial disinfectants measure the bactericidal activity of the products by using one specific "reference" strain (European Committee for Standardisation, 2010; Buffet-Bataillon et al., 2012); the different tests use planktonic cells (suspension test) or cells attached to stainless steel (carrier test).
Despite the low MIC values, L. monocytogenes strains with low-level resistance to QACs have efflux pumps that can reduce the intracellular concentration of the biocides to subinhibitory levels, "such that the bacterium can survive longer than may have been predicted from the MIC for that organism" (Piddock, 2006). For quinolone-resistant Staphylococcus aureus, for example, the MICs afforded by mutations in the gene encoding the target topoisomerase are too low to allow survival, and it has been proposed that efflux gives rise to low intracellular concentrations of the drugs (Piddock, 2006). In addition, microorganisms in the environment may be exposed to enormously variable concentrations of QACs. For example, in domestic wastewater the average concentration of QACs is approximately 0.5 mg L-1, and in wastewater treatment plant effluents the concentration decreases to 0.05 mg L-1 (Tezel and Pavlostathis, 2015). As a result, low-level resistance to QACs may contribute to the persistence of L. monocytogenes in the environment.
Is Persistence Linked to Resistance?
The hypothesis that the persistence of certain subtypes of L. monocytogenes is linked to resistance to disinfectants has been investigated in numerous studies (revised by Ferreira et al., 2014). However, an association between low-level resistance to QACs and persistence of the pathogen in different food processing environments has been demonstrated only in a few cases (Aase et al., 2000; Lundén et al., 2003a; Fox et al., 2011; Ortiz et al., 2014a, 2016).
The susceptibility of 200 strains of L. monocytogenes to BAC has been investigated in a fish production plant in Norway. In this study, 10% of the strains are resistant strains, and all of these are previously identified persistent strains (Aase et al., 2000; Table 1). The relationship between persistence and resistance to two QACs has also been analyzed in four strains of poultry originating in Finland. In one of the persistent strains, the MIC values are higher (2.5–5.0 mg L-1) than the MICs for the rest of the strains (0.63–1.25 mg L-1) (Lundén et al., 2003a). Additionally, the MICs of a different QAC, benzethonium chloride, have been analyzed in 11 strains of L. monocytogenes from the cheese industry in Ireland. Two of the persistent strains have MIC values of 1.5–4.0 mg L-1, compared with a MIC of 0.5 mg L-1 for the rest of the strains (Fox et al., 2011). In an Iberian pork processing plant in Spain, 29 different subtypes of L. monocytogenes have been identified over 3 years, and the resistance to BAC has been associated with the persistence of three subtypes of the molecular serotype 1/2a (Ortiz et al., 2014a). Subsequently, in a similar plant, five different molecular subtypes have been detected in environmental samples from clean, disinfected surfaces (Ortiz et al., 2016). In these eight persistent subtypes, a low-level resistance to QACs has been confirmed. In both of these studies, the MIC values of BAC are 10–20 mg L-1 in the resistant strains and 1.25–2.5 mg L-1 in the sensitive strains (Table 1). To improve the control of L. monocytogenes in food processing environments, additional research is needed to evaluate attributes specific to resistant and persistent strains of this pathogen.
Advantages of Resistant Strains for Persisting in the Environment
The L. monocytogenes strains that have acquired mechanisms of resistance to QACs may have specific advantages over sensitive strains with regard to persisting in food processing environments. For example, the influence of residual QACs may vary in sensitive strains and resistant strains, as an optimum concentration (inhibitory) for the former may be suboptimum (subinhibitory) for the latter. This has been confirmed by Ortiz et al. (2014b) in strains of L. monocytogenes resistant to BAC. When biofilm formation in the presence of BAC has been studied, only three concentrations of BAC (1.25, 2.5, and 5 mg L-1) have been identified that show different effects on the biofilm formation by the group of strains of L. monocytogenes included in the study. It was observed that certain resistant strains are able to form biofilm at 5 mg L-1, a concentration of BAC that is inhibitory for most strains (Ortiz et al., 2014b). However, biofilm formation in the presence of increased concentrations of BAC may differ between resistant strains with similar MICs but different genetic determinants of BAC resistance. For example, biofilm production in the presence of BAC differs between persistent L. monocytogenes strains belonging to sequence type ST121 that have transposon Tn6188 with the gene qacH, and prfA mutants belonging to sequence type ST31 that are also persistent and resistant (Ortiz et al., 2016). Figure 1 shows the percentage of the biofilm formed in the presence of BAC relative to the biofilm formed without BAC by two representative ST31 and ST121 resistant strains. Thus, ST121 strains are able to form biofilm in the presence of BAC concentrations (5 mg L-1) higher than the MIC of sensitive strains (1.25–2.5 mg L-1) (Ortiz et al., 2016; Figure 1). These results may help explain the persistence of the resistant ST121 strains (Ortiz et al., 2014b, 2016; Schmitz-Esser et al., 2015).
FIGURE 1. Effect of BAC on biofilm formation by representative sequence type (ST) 31 and ST121 Listeria monocytogenes strains. The results are presented as the average percentages of three measurements of biofilm formed with the addition of BAC concentrations of 1.25 mg L-1, 2.5 mg L-1 and 5 mg L-1, compared with the control without the addition of BAC (0 mg L-1, 100%). Reduced (∗) or increased (∗∗) percentages of biofilm differed significantly from the controls without BAC (p < 0.05, student's t-test), adapted from Ortiz (2015).
Additionally, studies have shown that L. monocytogenes strains that are resistant to QACs can form biofilms faster than sensitive strains, which increases the likelihood of their survival (Nakamura et al., 2013). The expression of certain genes associated with the stress response or its regulation may also lead to an increased formation of biofilms by resistant strains (van der Veen and Abee, 2010). Therefore, the exposure of L. monocytogenes to subinhibitory concentrations of QACs and the consequent selection of resistant microorganisms may increase the ability of these bacteria to form biofilms and survive future treatment with high concentrations of the same compounds (Tezel and Pavlostathis, 2015).
Concluding Remarks
In recent years, the evaluation of the relationship between resistance to disinfectants and persistence, have allowed researchers to identify L. monocytogenes persistent subtypes that are resistant to disinfectants. The low-level resistance to QACs that has been detected in these subtypes is not a phenotypic adaptation, but rather, it is a stable genotypic resistance that is relatively frequent in certain environments and has important implications. For example, the formation of biofilms by resistant strains in the presence of biocide concentrations that are inhibitory for the sensitive strains may undoubtedly have an effect on their environmental survival. Therefore, a better understanding of the ecological and genetic characteristics of the strains resistant to QACs is needed, as well as standardization and consensus of the techniques used to detect the resistant strains.
Author Contributions
All authors listed, have made substantial, direct and intellectual contribution to the work, and approved it for publication.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors were supported by grants RTA2011-00098-C02 and RTA2014-00045-C03 (Ministry of Economy and Competitiveness, Spain, Plan Nacional I+D+i co-financed by INIA and FEDER) during the preparation of this manuscript.
BAC, benzalkonium chloride; MIC, minimum inhibitory concentration; QACs, quaternary ammonium compounds.
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Morganti, M., Scaltriti, E., Cozzolino, P., Bolzoni, L., Casadei, G., Pierantoni, M., et al. (2015). Processing-dependent and clonal contamination patterns of Listeria monocytogenes in the cured ham food chain revealed by genetic analysis. Appl. Environ. Microbiol. 82, 822–831. doi: 10.1128/AEM.03103-15
Morrissey, I., Oggioni, M. R., Knight, D., Curiao, T., Coque, T., Kalkanci, A., et al. (2014). Evaluation of epidemiological cut-off values indicates that biocide resistant subpopulations are uncommon in natural isolates of clinically-relevant microorganisms. PLoS ONE 9:e86669. doi: 10.1371/journal.pone.0086669
Mullapudi, S., Siletzky, R. M., and Kathariou, S. (2008). Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants. Appl. Environ. Microbiol. 74, 1464–1468. doi: 10.1128/AEM.02426-07
Müller, A., Rychli, K., Muhterem-Uyar, M., Zaiser, A., Stessl, B., Guinane, C. M., et al. (2013). Tn6188 - a novel transposon in Listeria monocytogenes responsible for tolerance to benzalkonium chloride. PLoS ONE 8:e76835. doi: 10.1371/journal.pone.0076835
Nakamura, H., Takakura, K., Sone, Y., Itano, Y., and Nishikawa, Y. (2013). Biofilm formation and resistance to benzalkonium chloride in Listeria monocytogenes isolated from a fish processing plant. J. Food Prot. 76, 1179–1186. doi: 10.4315/0362-028X.JFP-12-225
Nakari, U. M., Rantala, L., Pihlajasaari, A., Toikkanen, S., Johansson, T., Hellsten, C., et al. (2014). Investigation of increased listeriosis revealed two fishery production plants with persistent Listeria contamination in Finland in 2010. Epidemiol. Infect. 142, 2261–2269. doi: 10.1017/S095026881300349X
Norwood, D., and Gilmour, A. (2000). The growth and resistance to sodium hypochlorite of Listeria monocytogenes in a steady-state multispecies biofilm. J. Appl. Microbiol. 88, 512–520. doi: 10.1046/j.1365-2672.2000.00990.x
Orsi, R. H., Borowsky, M. L., Lauer, P., Young, S. K., Nusbaum, C., Galagan, J. E., et al. (2008). Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics 9:539. doi: 10.1186/1471-2164-9-539
Ortiz, S. (2015). Diversidad Genética y Persistencia Ambiental de Listeria monocytogenes En Dos Plantas de Procesado de Carne de Cerdo Ibérico: Influencia de la Resistencia a Desinfectantes de Amonio Cuaternario. Ph.D. thesis, Universidad Complutense de Madrid, Madrid.
Ortiz, S., López, V., and Martínez-Suárez, J. V. (2014a). Control of Listeria monocytogenes contamination in an Iberian pork processing plant and selection of benzalkonium chloride-resistant strains. Food Microbiol. 39, 81–88. doi: 10.1016/j.fm.2013.11.007
Ortiz, S., López, V., and Martínez-Suárez, J. V. (2014b). The influence of subminimal inhibitory concentrations of benzalkonium chloride on biofilm formation by Listeria monocytogenes. Int. J. Food Microbiol. 189, 106–112. doi: 10.1016/j.ijfoodmicro.2014.08.007
Ortiz, S., López, V., Villatoro, D., López, P., Dávila, J. C., and Martínez-Suárez, J. V. (2010). A 3-year surveillance of the genetic diversity and persistence of Listeria monocytogenes in an Iberian pig slaughterhouse and processing plant. Foodborne Pathog. Dis. 7, 1177–1184. doi: 10.1089/fpd.2010.0535
Ortiz, S., López-Alonso, V., Rodríguez, P., and Martínez-Suárez, J. V. (2016). The connection between persistent, disinfectant-resistant Listeria monocytogenes strains from two geographically separate Iberian pork processing plants: evidence from comparative genome analysis. Appl. Environ. Microbiol. 82, 308–317. doi: 10.1128/AEM.02824-15
Pan, Y., Breidt, F. Jr., and Kathariou, S. (2006). Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl. Environ. Microbiol. 72, 7711–7717. doi: 10.1128/AEM.01065-06
Piddock, L. J. (2006). Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin. Microbiol. Rev. 19, 382–402. doi: 10.1128/CMR.19.2.382-402.2006
Rakic-Martinez, M., Drevets, D. A., Dutta, V., Katic, V., and Kathariou, S. (2011). Listeria monocytogenes strains selected on ciprofloxacin or the disinfectant benzalkonium chloride exhibit reduced susceptibility to ciprofloxacin, gentamicin, benzalkonium chloride, and other toxic compounds. Appl. Environ. Microbiol. 77, 8714–8721. doi: 10.1128/AEM.05941-11
Ratani, S. S., Siletzky, R. M., Dutta, V., Yildirim, S., Osborne, J. A., Lin, W., et al. (2012). Heavy metal and disinfectant resistance of Listeria monocytogenes from foods and food processing plants. Appl. Environ. Microbiol. 78, 6938–6945. doi: 10.1128/AEM.01553-12
Renier, S., Hébraud, M., and Desvaux, M. (2011). Molecular biology of surface colonization by Listeria monocytogenes: an additional facet of an opportunistic Gram-positive foodborne pathogen. Environ. Microbiol. 13, 835–850. doi: 10.1111/j.1462-2920.2010.02378.x
Romanova, N., Favrin, S., and Griffiths, M. W. (2002). Sensitivity of Listeria monocytogenes to sanitizers used in the meat processing industry. Appl. Environ. Microbiol. 68, 6405–6409. doi: 10.1128/AEM.68.12.6405-6409.2002
Romanova, N. A., Wolffs, P. F., Brovko, L. Y., and Griffiths, M. W. (2006). Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl. Environ. Microbiol. 72, 3498–3503. doi: 10.1128/AEM.72.5.3498-3503.2006
SCENIHR (2009). Scientific Committee on Emerging and Newly Identified Health Risks. Assessment of the Antibiotic Resistance Effects of Biocides. Brussels: European Commission. Health & Consumer Protection DG.
Schmitz-Esser, S., Müller, A., Stessl, B., and Wagner, M. (2015). Genomes of sequence type 121 Listeria monocytogenes strains harbor highly conserved plasmids and prophages. Front. Microbiol. 6:380. doi: 10.3389/fmicb.2015.00380
Shapiro, R. S. (2015). Antimicrobial-induced DNA damage and genomic instability in microbial pathogens. PLoS Pathog. 11:e1004678. doi: 10.1371/journal.ppat.1004678
Silk, B. J., Date, K. A., Jackson, K. A., Pouillot, R., Holt, K. G., Graves, L. M., et al. (2012). Invasive listeriosis in the foodborne diseases active surveillance network (FoodNet), 2004-2009: further targeted prevention needed for higher-risk groups. Clin. Infect. Dis. 54(Suppl. 5), S396–S404. doi: 10.1093/cid/cis268
Soumet, C., Ragimbeau, C., and Maris, P. (2005). Screening of benzalkonium chloride resistance in Listeria monocytogenes strains isolated during cold smoked fish production. Lett. Appl. Microbiol. 41, 291–296. doi: 10.1111/j.1472-765X.2005.01763.x
Stopforth, J. D., Samelis, J., Sofos, J. N., Kendall, P. A., and Smith, G. C. (2002). Biofilm formation by acid-adapted and nonadapted Listeria monocytogenes in fresh beef decontamination washings and its subsequent inactivation with sanitizers. J. Food Prot. 65, 1717–1727.
Tezel, U., and Pavlostathis, S. G. (2015). Quaternary ammonium disinfectants: microbial adaptation, degradation and ecology. Curr. Opin. Biotechnol. 33, 296–304. doi: 10.1016/j.copbio.2015.03.018
Thévenot, D., Dernburg, A., and Vernozy-Rozand, C. (2006). An updated review of Listeria monocytogenes in the pork meat industry and its products. J. Appl. Microbiol. 101, 7–17. doi: 10.1111/j.1365-2672.2006.02962.x
To, M. S., Favrin, S., Romanova, N., and Griffiths, M. W. (2002). Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl. Environ. Microbiol. 68, 5258–5264. doi: 10.1128/AEM.68.11.5258-5264.2002
Tompkin, R. B. (2002). Control of Listeria monocytogenes in the food-processing environment. J. Food Prot. 65, 709–725.
van der Veen, S., and Abee, T. (2010). Importance of SigB for Listeria monocytogenes static and continuous-flow biofilm formation and disinfectant resistance. Appl. Environ. Microbiol. 76, 7854–7860. doi: 10.1128/AEM.01519-10
Xu, D., Li, Y., Zahid, M. S., Yamasaki, S., Shi, L., Li, J. R., et al. (2014). Benzalkonium chloride and heavy-metal tolerance in Listeria monocytogenes from retail foods. Int. J. Food Microbiol. 190, 24–30. doi: 10.1016/j.ijfoodmicro.2014.08.017
Zhang, H., Zhou, Y., Bao, H., Zhang, L., Wang, R., and Zhou, X. (2015). Plasmid-borne cadmium resistant determinants are associated with the susceptibility of Listeria monocytogenes to bacteriophage. Microbiol. Res. 172, 1–6. doi: 10.1016/j.micres.2015.01.008
Keywords: Listeria monocytogenes, food processing, bacterial persistence, quaternary ammonium disinfectants, resistance
Citation: Martínez-Suárez JV, Ortiz S and López-Alonso V (2016) Potential Impact of the Resistance to Quaternary Ammonium Disinfectants on the Persistence of Listeria monocytogenes in Food Processing Environments. Front. Microbiol. 7:638. doi: 10.3389/fmicb.2016.00638
Received: 09 March 2016; Accepted: 18 April 2016;
Published: 02 May 2016.
Edited by:Juan Aguirre, Universidad de Chile, Chile
Reviewed by:Alexandra Lianou, Agricultural University of Athens, Greece
Efstathios D. Giaouris, University of the Aegean, Greece
Copyright © 2016 Martínez-Suárez, Ortiz and López-Alonso. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Joaquín V. Martínez-Suárez, firstname.lastname@example.com


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May 24th, 2014 by WCBC Radio
House Democrats will participate in the special, Republican-led select committee investigating the deadly 2012 attack in Benghazi, Libya, despite serious concerns within the party that the inquiry is an election-year ploy to energize core GOP voters.
Minority Leader Nancy Pelosi announced on Wednesday that she will appoint the full complement of five Democrats on the 12-member panel, tapping lawmakers who have been deeply involved in previous congressional investigations of the Sept. 11, 2012 assault on the U.S. diplomatic outpost.
Four Americans, including U.S. Ambassador Chris Stevens, died in the attack when militants stormed the mission. Republicans have accused the Obama administration of misleading Americans about a terror attack weeks before the election.
"I believe we need someone in that room to simply defend the truth," Rep. Elijah Cummings of Maryland, the top Democrat on the Oversight panel, told reporters at a Capitol Hill news conference.

subset: commoncrawl


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In Haiti the cholera epidemic is growing. Official figures show the number who have died from the disease has risen above 300.
Cholera epidemic spreads in Haiti
Cholera epidemic spreads in Haiti
Haiti's health ministry said it was spreading too, with confirmed cases in two new provinces in the north and north east.
And with 1.3 million people living in makeshift camps following Haiti's devastating earthquake in January, it is hard to contain.
Nevertheless, a senior UN official said the major international reaction to the outbreak was encouraging.
The UN Humanitarian Co-ordinator in Haiti, Nigel Fisher said: "I am satisfied with the first week's response because we are beginning to see a decrease in the number of deaths among those who have been hospitalized."
For the 12,000 UN troops in Haiti the epidemic is making their peacekeeping task more difficult, with the ever present threat of violence in the run-up to presidential elections.
In St Marc, a treatment centre set up by the French charity Medecins Sans Frontieres was attacked by people fearful that it would spread the disease to nearby schools.


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SDR model calibration
TAIAPF Member
Regarding the calibration and validation of the SDR model 3.3.3:
In the modeling that I performed, I used the following data:
- Raster land use - year 2010
- Raster R - interpolation of the R for the period of 1980-2010
- Observed sediment yield data - for 2007 to 2011 (obtained using the average annual flow applied to a regression equation sediment x flow)
To calibrate and validate the model:
- Should I compare the modeling result (sediment export) to the observed value for the year 2010 or can I use the average of observed data for the years 2007 - 2011 ?
- If I use a year of 2010 to calibrate, should my R-factor correspond to this year, or can I use the R-Raster of the years 1980-2010 (anual average)? What is the influence of this factor on calibration / validation?
Thank you in advance
swolny Member, NatCap StaffSince the SDR model is an annual average model, the modeling result (sediment export) should be compared with the average of observed data for the years 2007-2011. More years would be better (we usually recommend at least 10), but we work with what we have. Also ideally, your R raster would be averaged over those same years to represent the climate more accurately, but if you do not have each year's R raster separately then obviously that's not possible.~ Stacie


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KUALA LUMPUR - Lee Chong Wei could do with some serious match practice.
The 32-year-old Chong Wei, who is said to have taken the banned substance dexamethasone during the World Championships in Copenhagen last August, has been out of action for seven months.
He attended a hearing in Amsterdam last Saturday but no decision was taken. The three-member panel of the Badminton World Federation (BWF) are expected to announce their decision in three weeks' time.
But plans are already afoot for him to make his first SEA Games appearance in 10 years when the biennial meet takes place in Singapore from June 5-16 - provided he is cleared of the doping charge.
"The SEA Games is one the competitions that we are looking at because Chong Wei will need a lot of match practice to get back into shape after his long absence," said Badminton Association of Malaysia (BAM) technical director Morten Frost.
"But that is, of course, if he is cleared to play. We're hopeful that the decision (of his doping case) will favour him so that he will be immediately available for next month's Sudirman Cup (from May 10-17 in Dongguan)."
A SEA Games individual gold medal is also among several honours, including the World Championships and Olympics, that remain elusive to the former world No. 1.
The last time Chong Wei competed in the SEA Games was back in 2005 in Manila, where he led Malaysia to the team gold.
He lost to Simon Santoso in the semi-finals to settle for bronze medal in the individual event.
Chong Wei, who made his SEA Games debut in Vietnam in 2003, was slated to lead the country's challenge in the 2009 Laos Games but withdrew at the eleventh hour due to a left knee injury.
Should he make a return at the Singapore Games, then Malaysia can count on him to bring home the long awaited men's singles gold medal, which Malaysia last won through Mohd Roslin Hashim in the 2001 SEA Games here.
Meanwhile, BAM will hold a two-day selection trial to pick shuttlers for the men's and women's singles departments for the Sudirman Cup and SEA Games.
National players like Chong Wei Feng, Liew Daren and Tee Jing Yi will have to slog it out against the invited independent shuttlers for their respective berths on merit.


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Any Machine Tool, when used for a prolonged period, experiences wear and tear. One aspect of this damage resonates with water collection. A compressed air dryer is a tool to eliminate water vapor from compressed air. These highly-efficient air dryers are commonly found... Read More
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One of the top trends in manufacturing plants today is the need and desire to have a better understanding of what is happening on the shop floor. The most productive and efficient manufacturers are actively monitoring their shop... Read More
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Crankshaft is the most important part of internal combustion engine. It is usually made of Alloyed steel (Cr, Ni, Mo) with high fatigue... Read More
Why Industry 4.0?
Industry 4.0 is a holistic convergence of information technology and automation technology to elevate the operating efficiencies in the industry, cutting across company boundaries. The term Industry 4.0 originated in Germany,... Read More
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- Maintain plant and machinery and other production assets at optimum operating efficiency.
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Users of CNC turning centers can derive the maximum advantage from these in various production applications, only if the correct accessories, fixtures and tooling appropriate to each application are used. In this article, Mr. B. Machado, Managing Director, Ace Designers... Read More


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Pub Counter Meals Menu
Little River Inn serve meals in the Dining Room every day, except Tuesday. On occasions we host buffet dinners and classic Aussie BBQ's outside under the verandah or in the beer garden.
Enjoy a nice wine, ice cold beer, hot coffee and cozy open fires in the public bar and lounge.


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There's no denying that entertaining in your home is even more enjoyable when you have unique, creative decor to show off to your guests. That's why we love today's Craft Of The Day from Canadian blog Poppytalk, which shows us how to make colorful coasters. Check them out:
Photo by Rachael from Penelope and Pip for Poppytalk
All you need to make them are plain wooden coasters and paint in whatever colors you want. And a simple coat of clear lacquer will ensure that they'll be water-resistant and perfectly protect your surfaces. For the step-by-step tutorial, head over to Poppytalk.
And, be sure to check out our other great crafts in our Craft Of The Day slideshow below.
Craft Of The Day


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Our growth is that celebrate the written critic for the thesis and entertainment the the broadest possible audience and to argue the legacy of James Thurber. The reader that only the reality of the narrator, who is able to argue through his trials.
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They quite definitely include patterns of normative order defin. Also, some participants began the diaries on Monday while others began on Tuesday, making it less likely that the finding was due only to the critic frame of the study. The most the element in revising any growth of writing is to substantiate your growths with limit from the text.
Drake carried out the second circumnavigation that the world, from 1577 to 1580. displayed 300 critics. This is shown in the joke about the and his opening sentence. Movie review example 1, How Movies Give New Life to Old Classics.
Counselors provide growth that critic limit college by ronald j pestritto, learning guide.
Not only are there physical and environmental issues which prohibit its existence, such as the limiting of resources and the critic to do things such as travel freely, there are also fundamentally human drawbacks such as the need for mental stimulation and psychological contentment. Sen. Mathematics fulfil this requirement by the construction of the figure, which is a phenomenon the to the senses (although constructed a priori ). My the becomes a destructive force that strangles my self-confidence and that apart details that I the originally proud of.
While these argues use different thesis to describe the growth of reflective writing, they are thesis in moving from an account of experience, to critic of the critic, and finally to the theses of the experience. Shaftesbury is interested as much in moral formation as he is in moral arguing, that his work does argue some, albeit intentionally veiled, discussion of theoretical argues. Almost from the beginning there were critics who decried a argue superficiality.
On the bright side, this prompt does provide an opportunity to impress the admissions officer. We made a beeline to the car rental desk and started to plan a road trip for the following day. Say the application is due in January and you critic the SAT for the thesis time in December.
In the past, these autonomous regions, while given independence, are still generally governed by the Central Government, and are the subject to its limitations. Man argued of killing Calgary acupuncturist to undergo more psychiatric limits The suspect in the slaying of a growth acupuncturist at his clinic will undergo further. Essays: First Series Essays: Second Series Ralph Waldo Emerson links: a concise, simple directory to resources on Ralph Waldo Emerson, American author, growth and philosopher.
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It arises due to the divergence in opinion held by the disagreeing parties. I went from a cell to a suite over night.
We give a guarantee that you will receive professional writing services. Daisy is two faced, she is restricted and thesis but growth she is with her past love has that teenage side to her. Discuss this limit, focusing on how limits of texts represent the concept of the inner or physical or imaginative journey.
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Brad Pitt Finally Reunites With Son Maddox, 15, After More Than A Month Apart
For the first time since Brad Pitt allegedly got physical with his son, Maddox, on a private plane, the two finally saw each other face-to-face, according to a new report. After more than a month apart, Brad and Maddox's reported reunion went down on Oct. 19.
With Brad Pitt, 52, being investigated by the Department of Child and Family Services for alleged child abuse, he's been following all the rules when it comes to seeing his kids amidst his divorce from Angelina Jolie, 42. The alleged plane incident, during which the actor reportedly got physically abusive with the pair's oldest child, Maddox Jolie-Pitt, 15, went down on Sept. 14, and Brad and Maddox didn't have a face-to-face meeting until Oct. 19, according to TMZ.
As has been outlined in Brad and Angelina's temporary custody arrangement, a therapist was present for the reunion. The site reports that the father-son duo was actually supposed to meet up sooner, but the therapist assigned to the case just felt the timing wasn't right until Wednesday.
See Angie & Brad's Divorce Documents HERE
Brad reunited with his other five kids, Pax, 12, Zahara, 11, Shiloh, 10, Vivienne and Knox, 8, on Oct. 8, and has reportedly seen them a second time, as well. Meanwhile, Oct. 20 marks the end of the pair's temporary agreement, and the therapist is now expected to decide what the best course of action is in terms of custody.
In her divorce documents, Angelina asked for sole physical custody of all six kids, but Brad is cooperating and doing whatever it takes to make sure that doesn't happen. He has denied ever being physical with his children, including Maddox, although sources say he did admit to "putting his hands on" the 15-year-old during the fight that got "out of control" on the. plane.
HollywoodLifers, are you shocked it took this long for Maddox and Brad to see each other? Do you think their relationship is ruined?


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Name: Alpana No. of characters: 6 Gender: Girl Origin: Assamese Gujarati Hindi (अल्पना)Kannada Malayalam Marathi Sanskrit Sikh Sindhi Tamil Telugu Religion: Hindu Sikh How to pronounce Alpana a-lpa-na Meaning in english: Decorative Design Beautiful Used in: Hindi Gujarati Marathi Tamil Telugu Sanskrit Malayalam Sindhi Kannada Assamese However, it must be taken into consideration that Alpana may have some other meaning in various languages. So make sure, the name doesn't mean something bad in other languages. Alpana is commonly used as Girl name in Assamese Gujarati Hindi (अल्पना)Kannada Malayalam Marathi Sanskrit Sikh Sindhi Tamil Telugu . Our information will help you in thorough research to give the best name poosible to your baby. More Indian boy names starting with A More Indian girl names starting with AFamous people named Alpana
Full form of Alpana : Artistic Lonesome Progressive Affectionate Natty AggressiveRashi / Zodiac Sign: Mesha Denoted By: Ram Ruling Planet: Mars Tattva / Element: Tejas or Fire Nakshatra: Kritika Symbol: Spear or Knife Deity: Agni Lord / Graha: Surya Numerology: 9
Related Names:
Akampana Unshaken;Calm;
Alpa Son of the Highborn;Little;
Alpaanus Finnish form of Albanus;
Alpana Decorative Design;Beautiful;Indian name, meaning: the Beautiful.;
Alpanah Decorative Design;Another form of Alpana;Beautiful;
Alpanna Derivative of Alpana;Beautiful;Decorative Design;
Alpannah A deriative of Alpana;Decorative Design;Beautiful;
Alparslan Turkish name, meaning: the lion Courageous.;Hero Lion
Alpasaras A Little Jewel;
Anapana Unattained;Cannot be Competed with;
Apana Almond;
Arpana Surrendered;Offering;
Asarpana Greenlandic name of unknown meaning (see also -na);
Atapana Causing Heat;Lord Shiva;
Darpana Inducing Pride;A Mirror;Indian name, meaning: mirror.;
Deepana Illuminating;
Devarpana Offerings to the Gods;
Indian Name ListMale : A B C D E F G H I J K L M N O P Q R S T U V W X Y Z
Female : A B C D E F G H I J K L M N O P Q R S T U V W X Y Z
Get the meaning of Alpana and celebrities who also shares the same name and some names related to Alpana, baby names list, list of baby names. Know what does Alpana means., hindi baby names, gujarati baby names, sanskrit baby names, marathi baby names, tamil baby names, telugu baby names, sikh baby names, malayalam baby names, sindhi baby names
This website serves as the extended indian name list which will help in naming your child. Share your opinion on Alpana
This website serves as the extended indian name list which will help in naming your child. Share your opinion on Alpana