Listeria monocytogenes in Food-Processing Facilities,Food Contamination,and Human Listeriosis: The Brazilian Scenario

Introduction

Consumption of food and water contaminated by microorganisms is associated with the morbidity and mortality of humans worldwide (World Health Organization, 2007). Listeria monocytogenes is a foodborne pathogen that is frequently isolated from a variety of food-processing environments and food products. Its prevalence in food processing facilities is attributable to its resistance to environmental stress, ability to multiply at low temperatures, and ability to form biofilms on the surfaces of different sites in processing facilities (Ryser and Marth, 2007; Swaminathan and Gerner-Smidt, 2007; Carpentier and Cerf, 2011).

Ingestion of foods contaminated by L. monocytogenes can lead to listeriosis in people and other mammals. Although this disease can occur in healthy individuals, the invasive form is more likely to affect neonates, pregnant women, elderly, and immunocompromised individuals. The incidence of listeriosis is lower than other foodborne pathogens; however, the disease presents a high fatality rate, placing L. monocytogenes among the main foodborne pathogens that cause deaths in the United States (Scallan et al., 2011, 2015). In Brazil, however, the scenario is different: many studies demonstrate the presence of L. monocytogenes in food processing environment and in food products, but little is known about the incidence of human listeriosis, most probably due to the absence of an efficient surveillance and notification system (Lemes-Marques et al., 2007; Blum-Menezes et al., 2013).

Control of L. monocytogenes in food processing facilities is a challenge, in part, because this pathogen can persist for years in these facilities. Nevertheless, the adoption of proper sanitization practices is the best way to control the pathogen in food processing facilities and avoid cross-contamination to end products. This review focuses on describing the distribution of L. monocytogenes in the food processing environment, food contamination, the consequences for human health due to ingestion of contaminated foods, and the control of L. monocytogenes by food industries, comparing data obtained in Brazil with the international scenario.

L. monocytogenes Distribution and Food Contamination

L. monocytogenes is widely distributed in the natural environment and it can be isolated from soil, water, drainage systems, vegetation, animal feed, farm environments, food processing facilities, various foods, and feces from healthy animals, including humans (Ryser and Marth, 2007; Sauders et al., 2012). Several studies have documented the occurrence of L. monocytogenes in food processing facilities worldwide (Table 1). Many of these studies highlight the role of the food processing environment as sources of L. monocytogenes contamination of finished products.

Occurrence of L. monocytogenes on bovine carcasses, in beef processing environment, and on final cuts has been documented in different regions of Brazil. Barros et al. (2007) evaluated the occurrence of Listeria spp. and L. monocytogenes in 11 meat processing establishments, demonstrating that the pathogenic serotypes 1/2a and 4b are distributed on equipment and facilities in beef processing plants and meat products in the South of Brazil. Camargo et al. (2015b) studied the diversity of L. monocytogenes in a beef processing environment in the Southeastern region, demonstrating by pulsed-field gel electrophoresis (PFGE) that isolates recovered from final products shared the same profiles of isolates obtained from chopping boards and hands of employees.

Guerini et al. (2007) also detected Listeria spp. at four cull cow and bull processing plants in the United States. L. monocytogenes was detected on carcasses in the chill cooler, including the pathogenic serotypes 1/2a, 1/2c, and 4b. Serotype 1/2c isolates that were recovered in the summer of 2005 and spring of 2006 from plant “A” shared a high similarity by PFGE, suggesting they were persistent, similar as observed by Camargo et al. (2015b) in Brazil. Serotype 4b isolates that were found on hides and carcasses in the chill cooler presented different PFGE profiles, indicating they came from a different source.

Regarding the occurrence of L. monocytogenes in the pork chain, various studies demonstrated that L. monocytogenes is ubiquitous in the Brazilian processing industry (Silva et al., 2004; Miyasaki et al., 2009; von Laer et al., 2009; Rossi et al., 2011). Interestingly, the pork processing environment in Brazil seems to be a source of atypical L. monocytogenes serotypes (Miyasaki et al., 2009), as well as atypical hemolytic L. innocua (Moreno et al., 2012).

A 2-year long study was conducted by Larivière-Gauthier et al. (2014) in a pork slaughter and cutting plant in the Province of Quebec, Canada, to assess the distribution of L. monocytogenes. They found a high diversity of strains by PFGE within the entry areas of the processing plant (such as lairage pen environment, slaughtering, and evisceration), but overrepresentation of one PFGE type in the cutting room environment. A similar 3-year study (2008–2011) was conducted in five pork plants in Sardinia, Italy. Among 211 samples, L. monocytogenes was detected from swine carcasses (33%), cecal material (7%), dehairing equipment, knives, carcass splitter surfaces (23%), floor drains, and walls in the dirty zone (25%); only serotypes 1/2c (78%) and 1/2a (22%) were detected (Meloni et al., 2013). In another study from Italy, 23 of 774 carcasses (3%) and 94 of 752 fresh hams (12.5%) were positive for L. monocytogenes. Nevertheless, only 14 of 708 (2.0%) dry-cured hams presented positive results for the pathogen, consistent with less risk associated with dried products (Prencipe et al., 2012).

Despite having good manufacturing practices, control of L. monocytogenes in Brazilian poultry processing facilities remains a challenge (Barbalho et al., 2005; Chiarini et al., 2009). This challenge is not a particular problem only in Brazil: Berrang et al. (2010) studied a newly constructed chicken processing plant in the United States and did not detect L. monocytogenes before the beginning of operations; however, within 4 months of regular processing, different L. monocytogenes strains (as defined by PFGE) were identified in floor drains, both before and after cleaning and sanitizing operations. In another study, Chasseignaux et al. (2001) tracked L. monocytogenes isolates obtained from poultry and pork processing plants where they detected L. monocytogenes at multiple locations: PFGE profiles indicated that some strains were recovered from the plants for several months, while others were not recovered on subsequent visits during the period studied.

The fish processing environment is also a source of L. monocytogenes, and the consumption of contaminated smoked fish has been involved in listeriosis outbreaks. Gudmundsdóttir et al. (2005) detected L. monocytogenes contamination in cold-smoked salmon and the associated processing environment in Iceland, and found an overall prevalence of 11.3%, with 4% of final product being positive. The same strains, as identified by identical PFGE profiles, were also recovered from raw material, floors, and drains. Vongkamjan et al. (2013) identified persistent L. monocytogenes strains from a smoked fish processing facility in the United States. In another study conducted in the United States, the authors selected four smoked processing plants for sampling and three were positive for L. monocytogenes in raw fish and processing environments (Thimothe et al., 2004). Studies in fresh and processed “surubin,” a typical Brazilian fish, demonstrated low frequencies of L. monocytogenes and suggested the low risk of listeriosis associated with the consumption of this fish type (Alves et al., 2005; Souza et al., 2008).

Listeria monocytogenes has been a problem in dairy facilities (Ryser and Marth, 2007), with sequential detection between years in some cases (Almeida et al., 2013). Parisi et al. (2013) reported the occurrence of L. monocytogenes in 7 (20.6%) of 34 dairy plants studied in Italy. Barancelli et al. (2014) evaluated the occurrence L. monocytogenes in three cheese manufacturing plants in Brazil, and serotypes 4b, 1/2b, and 1/2c were detected in two plants, with serotype 4b being the most frequently recovered serotype: PFGE analysis indicated the presence of multiple strains and thus contamination may have arisen from multiple sources.

Studies over the past decades indicate that L. monocytogenes can contaminate and multiply in a variety of foods, even those with high salt content or that are stored at refrigerated temperatures. Ready-to-eat foods (RTE) are common vehicles involved in listeriosis outbreaks, stimulating many countries to create specific legislation aiming to control L. monocytogenes in these foods after the 1990s. In the United States, there is a zero tolerance policy for L. monocytogenes in RTE (Shank et al., 1996). Similarly, the Brazilian Ministry of Agriculture, Livestock and Food Supply (MAPA) adopted the criteria of the absence of L. monocytogenes in RTE in Brazil (MAPA, 2009). In Canada and in some European countries, the norms vary among food products: <100 colony-forming unit (CFU)/g is tolerated in foods that are not suitable for Listeria growth, and a zero tolerance standard was adopted for foods that support growth and that possess extended shelf life (European Commission, 2005, 2007; Canada Health, 2011).

Among 778 packaged smoked fish produced by 50 different manufacturers located in 12 European Union countries, 157 samples (20.2%) were contaminated by L. monocytogenes, however, only 26 samples (3.3%) at levels higher than 100 CFU/g (Acciari et al., 2017). An integrative survey carried out in Italy tested 2696 RTE samples (884 from soft and semisoft cheese and 1802 from cooked meat products), and the contamination of meat products was 1.66% at the arrival at the laboratory and 1.92% at the end of shelf-life, while the prevalence in cheese was 2.13% at the arrival and 1.01% at the end of shelf-life (Iannetti et al., 2016). The occurrence of L. monocytogenes was analyzed in 2864 RTE samples obtained in the Eastern region of Spain, with 3.8% tested as positive; the pathogen was more common in smoked salmon and dried pork sausage samples (Doménech et al., 2015). These studies indicate that noncompliance with EU official criteria (100 CFU/g) was obtained only from few samples; the hygiene management strategies applied by different manufacturers appear to result in different levels of contamination in the final products.

In Brazil, Sant'Ana et al. (2012) detected 3.1% (16/512) RTE vegetables marketed in São Paulo positive for L. monocytogenes, and only five samples presented countable levels, with counts ranging from 1.0 × 10¹ to 2.6 × 10² CFU/g. A similar prevalence was observed by Byrne et al. (2016) in RTE vegetables commercialized in Salvador. In another study carried out in Brazil, Martins and Leal Germano (2011) found 6.2% salami samples and 0.8% ham samples positive for L. monocytogenes. Counts in salami samples ranged from <10 to 1900 CFU/g, and the results suggest that consumption of salami can be associated with high risk of listeriosis in the consumers. The distribution of Listeria spp. and L. monocytogenes serotypes in food samples collected in Brazil between 1990 and 2012 was analyzed recently by Vallim et al. (2015), and the pathogenic serotypes 1/2a, 1/2b, and 4b were the most common in nonprocessed meat, while serotypes 1/2a and 4b were the most commonly found in processed meat and RTE.

The Brazilian legislation allows reprocessing the RTE animal products positive for L. monocytogenes, since the procedure applied ensures the destruction of the pathogen. After the reprocessing, the establishments must carry out a microbiological analysis to ensure that L. monocytogenes is absent. In addition, after detection of L. monocytogenes in RTE foods, the supervised establishments shall review their self-control procedures (MAPA, 2009).

Based on the presented information, different steps from the food processing environment can be considered relevant sources of L. monocytogenes contamination in foods. Then, listeriosis development is clearly linked to consumption of contaminated foods and also to particular characteristics of the consumer and virulence of L. monocytogenes.

Epidemiology of Human Listeriosis

Listeria monocytogenes incidence is much lower (0.2/100,000 people globally) compared to other enteric pathogens, such as Salmonella enterica (1140/100,000), enterotoxigenic Escherichia coli (1257/100,000), and Campylobacter spp. (1390/100,000) (Kirk et al., 2015). The WHO evaluated the median rate of listeriosis in different regions in 2010 and estimated that the incidence of listeriosis is similar across different regions (was 0.1/100,000 people in Africa, Eastern Mediterranean, and South-East Asia; 0.2/100,000 people in Europe and the Western Pacific; and 0.3/100,000 people in the Americas) (Kirk et al., 2015). Interestingly, in some Northern European countries, the incidence rate has been higher (0.6–1.6 cases/100,000 people) than in other countries in recent years, maybe due to the increased consumption of RTE meat and fish products (Jensen et al., 2010; EFSA, 2012). Less is known about the outcome of listeriosis cases, although de Noordhout et al. (2014) estimated that listeriosis resulted in 23,150 illnesses and 5463 deaths globally in 2010.

Listeriosis cases and outbreaks have been described in multiple countries since 2000s (Table 2), with different foods involved as vehicles, including cantaloupe, caramel apples, RTE salad, dairy products, diced celery, meat products, fish products, cooked ham, and deli meat, among other foods. In 2013 alone, the 27 member states of EU reported 1763 confirmed human cases of listeriosis, resulting in 191 deaths (EFSA, 2015). Listeriosis can manifest itself invasively or not, and it is responsible for a high hospitalization rate (95%). Mortality rates can range between 20% and 30%, and serotypes 1/2a, 1/2b, and 4b are involved in more than 95% of the cases and outbreaks. The invasive form demands rapid antibiotic treatment and is characterized by severe infection in persons belonging to risk groups (Swaminathan and Gerner-Smidt, 2007). Unfortunately, hospitals themselves can be a significant source of listeriosis because of the combination of access to RTE foods and a higher probability of consumers who are immunosuppressed (Silk et al., 2014).

According to Todd and Notermans (2011), products such as soft cheeses and deli meats were commonly involved in listeriosis outbreaks around the world. Similar transmission vehicles were observed by Cartwright et al. (2013), where the authors reported changes in characteristics of outbreaks reported in the United States by CDC during 1998–2008. Earlier in the study period (1998–2003), the outbreaks were generally larger and longer in comparison with the late period (2005–2008). In the United States, declining cases may reflect the efforts of PulseNet to quickly identify and stop outbreaks. However, Salmonella and L. monocytogenes are still the major bacterial foodborne pathogens leading to death in the United States (Scallan et al., 2011, 2015).

The first documented North American outbreak of listeriosis (1981) linked to the consumption of contaminated coleslaw happened in Nova Scotia, Canada, with 41 cases and 18 deaths (Schlech et al., 1983). In 1983, there was an outbreak in Massachusetts, United States, with 49 cases and 14 deaths, linked to pasteurized milk (Fleming et al., 1985). A large listeriosis outbreak occurred in Southern California, United States, in 1985 with 142 cases and 48 deaths, caused by consumption of a soft cheese (Linnan et al., 1988). Other relevant outbreaks happened before the 2000s, for example, between 1983 and 1987 in Switzerland (with 122 cases and 34 deaths), in United Kingdom between 1987 and 1989 (total of 366 cases), in France during 1992 (279 cases and 85 deaths), and in the United States between 1998 and 1999, with 108 cases and 14 deaths (Swaminathan and Gerner-Smidt, 2007).

Large outbreaks have become less frequent since 2000s, presumably due to implementation of Listeria control measures by the food industry and improved clinical diagnostics. Unlike the 1980s and 1990s when L. monocytogenes was commonly recovered from the central nervous system (Mylonakis et al., 1998), currently the pathogen is most often detected in the blood, probably due to advances in medical diagnoses. The serotype 4b is most often responsible for meningoencephalitis, and it has also becoming less prevalent (Swaminathan and Gerner-Smidt, 2007), but according to Cartwright et al. (2013), this serotype is still responsible for the largest number of outbreaks in the United States. However, in Canada and European countries, the serotype 1/2a has become more common (Knabel et al., 2012; Mammina et al., 2013; Althaus et al., 2014; Lomonaco et al., 2015; Jensen et al., 2016).

One factor that hampers investigations in many countries, including Brazil, is the absence of an effective surveillance system and a lack of reporting requirements. There are few registers of isolation of L. monocytogenes from clinical cases in Brazil, and as listeriosis is not a disease under compulsory notification, the outbreak investigation is very often compromised. Reis et al. (2011) reported that serotype 4b was the most frequently recovered serotype from clinical samples between 1969 and 2008 in Brazil, but serotypes 1/2a, 1/2b, 1/2c, 3a, 3b, 4a, and 4ab have all been found among clinical material of human origin in Brazil (Hofer et al., 2000, 2006). A cluster of listeriosis in hospitalized patients (caused by serotypes 1/2b and 3b) was characterized for the first time in Brazil by Martins et al. (2010), and the results indicate that the hospital kitchen was the possible source of contamination. To determine the true incidence of listeriosis in countries like Brazil, it is necessary for the implementation of a laboratory surveillance system to track sporadic cases or outbreaks of human listeriosis and the sources of contamination (Lemes-Marques et al., 2007; Blum-Menezes et al., 2013).

Clinical Manifestations, Treatment, and Monitoring of Resistance

The incubation period of L. monocytogenes ranges between 3 and 70 days according to observations by Linnan et al. (1988) from a large 1988 listeriosis outbreak. Goulet et al. (2013) recently demonstrated that incubation periods differed significantly by clinical form of the disease, the longer incubation periods being identified in pregnancy-associated cases (median 27.5 days), followed by infections in the central nervous system (median 9 days), sepsis (median 2 days), and febrile gastrointestinal disease (median 24 h). In pregnant women, infection is more frequent in the third trimester, generally asymptomatic or with mild symptoms. The consequences to the fetus or newborn are extremely serious, including stillbirth, premature birth, pneumonia, sepsis, and meningitis (Janakiraman, 2008). Early-onset neonatal listeriosis occurs in infants infected in utero. The late-onset type may occur from one to several weeks after birth, as the result of transplacental transmission, cross-contamination, or ingestion of contaminated foods (Ryser and Marth, 2007; Janakiraman, 2008).

Among immunocompromised patients, such as the elderly, transplant patients, and HIV carriers, and in people diagnosed with cancer, listeriosis can present as sepsis, meningitis, or meningoencephalitis. In immunocompetent individuals, noninvasive listeriosis is most common and manifests itself as febrile gastroenteritis, diarrhea, muscle pain, and headache (Ryser and Marth, 2007; Cartwright et al., 2013). Although L. monocytogenes is the only species considered pathogenic to humans, sporadic cases of gastroenteritis and bacteremia due to L. ivanovii (Guillet et al., 2010), bacteremia due to L. innocua and L. grayi (Perrin et al., 2003; Rapose et al., 2008), and meningitis due to L. innocua (Favaro et al., 2014) and L. seeligeri (Rocourt et al., 1986) have been reported in the last few years.

Regarding the treatment with antibiotics, L. monocytogenes is sensitive to most drugs suitable for Gram-positive bacteria with the most common treatment involving β-lactam antibiotics (penicillin or ampicillin), potentially in conjunction with gentamicin. Vancomycin and trimethoprim/sulfamethoxazole are alternative drugs for patients allergic to penicillin. In addition, erythromycin, tetracycline, chloramphenicol, rifampicin, and linezolid can be used. The choice of antibiotic will vary according to the symptoms of infection and patient risk group (Salamano et al., 2005; Swaminathan and Gerner-Smidt, 2007; Janakiraman, 2008).

In Brazil, Reis et al. (2011) reported only one strain (1.5%) resistant to rifampin, and two (3%) were resistant to trimethoprim–sulfamethoxazole among 68 human strains isolated between 1970 and 2008, but increase in the minimum inhibitory concentration values reinforces the need of continuing resistance surveillance. Lemes-Marques et al. (2007) observed two clinical strains resistant to sulfamethoxazole. In addition, a large number of strains resistant to clindamycin and oxacillin were reported by Camargo et al. (2015a) among isolates obtained from meat processing environments, beef products, and clinical cases in Brazil.

Listeria monocytogenes recovered from food and food processing environment can be resistant to antimicrobial agents, including drugs used for listeriosis treatment (Table 3). Similar as observed in Brazil, few strains obtained in European countries (from food, food processing environments, and clinical) have demonstrated resistance to key antimicrobials (Vitas et al., 2007; Conter et al., 2009; Granier et al., 2011; Korsak et al., 2012; Khen et al., 2015). However, description of resistance to antimicrobials that are not commonly used for listeriosis treatment appears to be increasing (Alonso-Hernando et al., 2012; Khen et al., 2015). In addition, multidrug-resistant strains have been isolated from RTE in different regions of the world, creating an concern about dissemination of these strains in the food processing chain (Chen et al., 2014; Doménech et al., 2015).

According to Magalhaes et al. (2014b), who characterized L. monocytogenes isolates from human clinical cases that occurred in Portugal between 2008 and 2012, resistance to ciprofloxacin, rifampicin, nitrofurantoin, and streptomycin was observed, with 29 isolates (14.3%) resistant to two or more antimicrobials of different classes. Even though the incidence of antibiotic-resistant isolates is relatively low, it was significantly higher than in previous years (2003–2007) (Barbosa et al., 2013). Morvan et al. (2010) evaluated 4816 L. monocytogenes isolates obtained from clinical cases in France, and the prevalence of resistance was estimated at 1.27%, the resistance to tetracyclines and fluoroquinolones being more common, and also the presence of resistance-related genes dfrD, tetM, int-Tn, cat, and lde. In the same study, the authors described the first clinical isolate exhibiting a high level of resistance to trimethoprim, and an increase in penicillin MICs, reinforcing the need of continuous surveillance.

L. monocytogenes efflux pumps encoded by lde are associated with fluoroquinolone resistance (Godreuil et al., 2003), while resistance to macrolides, cefotaxime, heavy metals, and ethidium bromide is encoded by mdrL (Mata et al., 2000). Mobile plasmids (pIP501, pAMβ1, pRYC16, pDB1, pIP811, pIP823, pUBX1, and pWDB100) and transposons (Tn1545-Tn916 family) from enterococci and streptococci may transfer antibiotic resistance genes to Listeria spp. Some of these mobile elements can be transferred among Listeria species once they are in the same environment (Charpentier et al., 1995; Biavasco et al., 1996; Roberts et al., 1996; Charpentier and Courvalin, 1999; Bertsch et al., 2013).

Tetracycline resistance from Listeria strains is most frequently associated with tet(M), which can be transferred to Listeria by mobile elements such as a family of conjugative transposon Tn916. The int-Tn gene is a target to detect the transposon family Tn916-Tn1545 (Bertrand et al., 2005; Bertsch et al., 2014; Haubert et al., 2016). In addition to the tet(M), others genes that mediate tetracycline resistance, such as tet(K), tet(L), and tet(S), can also be expected in L. monocytogenes (Poyart-Salmeron et al., 1992; Facinelli et al., 1993; Hadorn et al., 1993; Yan et al., 2010). The resistance genes dfrD (corresponding resistance to trimethoprim), spc (spectinomycin), and erm(A) (erythromycin or clindamycin) can be located on plasmids such as pDB2011 (Bertsch et al., 2013). Similarly, chloramphenicol resistance can be encoded by the cat gene carried on plasmids. According to Poyart-Salmeron et al. (1990), the genes carried on plasmid pIP811 confer resistance to chloramphenicol, erythromycin, and streptomycin. Haubert et al. (2016) recently identified L. monocytogenes isolates from food processing environment and food obtained in Brazil, exhibiting multidrug resistance phenotypes. Two multidrug-resistant strains harbored the tetM and ermB resistance genes, and the presence of resistance gene (tetM) in a plasmid indicates a potential risk of transferring multidrug resistance to other microorganisms.

The differences in the frequency of antibiotic resistance of L. monocytogenes strains between studies could be, in part, explained by design of experiments, number of strains tested, and biological independence. It is important to keep in mind that in many studies that focus on resistance to antibiotics, the authors do not use techniques such as PFGE, capable of distinguishing the tested isolates (Miranda et al., 2008; Conter et al., 2009; Camargo et al., 2015a; Obaidat et al., 2015; Loiko et al., 2016). Without attention to the possibility that investigators are sampling from clonal populations, estimates of the prevalence of antibiotic resistance over time (increasing or decreasing) may be biased by repeated characterization of the same strains.

Control of L. monocytogenes in food processing facilities

Eliminating L. monocytogenes from food processing environmental is nearly impossible; however, the implementation of control procedures by MAPA in 2009 was an important step to overcome the worse scenarios observed in the past (Destro et al., 1991; Silva et al., 1998; Catão and Ceballos, 2001; Padilha da Silva et al., 2004). Despite the low prevalence of L. monocytogenes in RTE worldwide, samples with counts above the limit allowed by the legislation can offer a high risk to consumers, and the risk tends to increases with the number of cells ingested.

The bacterial biofilms are important to the food industry because these structures provide an additional means to protect bacteria from sanitation efforts. The association between higher adherence and persistence of L. monocytogenes in industrial environments was identified by Norwood and Gilmour (1999). While some investigators have shown serotype-specific differences in biofilm formation, others have found no correlation, indicating that the ability to form biofilms varies by strain rather than by serotype (Norwood and Gilmour, 1999; Lundén et al., 2000; Djordjevic et al., 2002; Borucki et al., 2003; Di Bonaventura et al., 2008; Pan et al., 2010; Nilsson et al., 2011). In addition, a multispecies biofilm can be more resistant than a biofilm composed only by L. monocytogenes (Møretrø and Langsrud, 2004).

The best approach to avoid biofilm formation and food contamination is to adopt effective cleaning practices to remove organic matter that can be metabolized by the bacteria. Disinfection with quaternary ammonium compounds (QACs), sodium hypochloride, sodium dichloroisocyanurate, peracetic acid, and iodofors can be effective against L. monocytogenes. The processing environments must to be designed to accommodate complete removal of particulates during prewash, access of chemicals at proper concentrations, and the ability to completely rinse surfaces, such as interior of drains, floors, cut room, grinders, and boxes, among others (Ryser and Marth, 2007; Chaitiemwong et al., 2014).

QACs are applied in medical and food processing environments with benzalkonium chloride (BC), an usual formulation for sanitization. As chlorine is completely dissolved in water, it is widely used in food processing facilities, with the additional advantages of being easy to use, low cost and high antimicrobial activity. However, it is very important to know their functions, effective concentrations, action mode, and the correct way to prepare them to optimize their application, avoid health risks, and obtain a better effect with a minimal quantity. Silva et al. (2016) studied the Listeria spp. contamination in a butcher shop located in Minas Gerais, Brazil. The authors evaluated the L. monocytogenes adhesion ability and sensitivity to food contact surface sanitizers (chlorine-based and quaternary ammonium-based compounds). After the adoption of both sanitizers in the cleaning routine of the butcher shop, L. monocytogenes was not detected, demonstrating in situ their effectiveness and the importance of the adoption of appropriate sanitation procedures for L. monocytogenes control.

While effective, To et al. (2002) demonstrated that L. monocytogenes can survive sublethal concentrations of BC through the activity of efflux pumps; these mechanisms may contribute to higher tolerance of BC should advantageous mutations arise. QACs are not recommended for use on surfaces that come into direct contact with fermented food because small concentrations of residues can inactivate “starter” cultures. One alternative would be to use peracetic acid, which does not have this shortcoming.

In addition to the use of chemicals, development of alternative strategies to eliminate L. monocytogenes has become an active field of research. There are studies that describe the use of ultraviolet radiation, bacteriophages, lactic acid bacteria, purified bacteriocins produced by lactic acid bacteria, ultrasonic treatment, natural products (such oils), and surfactants to control L. monocytogenes in the food processing environment or directly in the food (Møretrø and Langsrud, 2004; Cotter et al., 2013; Giaouris et al., 2014; Camargo et al., 2015c; Strydom and Witthuhn, 2015; Baños et al., 2016).

Although many bacteriocins produced by lactic acid bacteria have been characterized, their application by food industries is still restricted and can vary by country (Cotter et al., 2005; de Arauz et al., 2009; Favaro et al., 2015). In Brazil, studies have been describing bacteriocinogenic strains with an antilisterial activity isolated from raw milk and cheeses (Perin et al., 2012; Cavicchioli et al., 2017), sausage (De Martinis and Franco, 1998), salami (Barbosa et al., 2014), charqui (Biscola et al., 2013), pork products (de Carvalho et al., 2010), rocket salad (Kruger et al., 2013), and smoked fish (Alves et al., 2005).

The restrictions for the use of these bacteriocins can be, in part, explained because some producer strains are often considered nonsafe or the data available about these bacteriocins are still insufficient to approve their use, since this characterization is expensive and time-consuming. Nisin was the first approved bacteriocin for control of L. monocytogenes. Currently, nisin (a lantibiotic, class I bacteriocin) and pediocin Pa1/AcH (class IIa antilisterial bacteriocins) are approved and used to treat many types of food worldwide, while others bacteriocins produced by acid lactic bacteria offer promising perspectives to be approved for commercial use (Gálvez et al., 2007; López Aguayo et al., 2016).

Various phage preparations also have been successfully tested against L. monocytogenes in the last years. The ListShield^™ was the first phage-based preparation approved by the Food and Drug Administration and the Environmental Protection Agency. Since then, the product was approved by others countries to be used as decontaminant of surfaces and equipment and direct on food. In addition, the LISTEX^™ P100 has been tested and approved in several countries (Carlton et al., 2005; FDA, 2014; Gutiérrez et al., 2017; Yang et al., 2017). The efficiency of bacteriophage P100 (LISTEX P100) was evaluated by Rossi et al. (2011), being demonstrated that this product was very effective for biocontrol of L. monocytogenes in Brazilian fresh sausage. Bacteriophages can be useful for L. monocytogenes biocontrol in food contact surfaces and in foods; however, dose, contact time, storage temperature, and pH potentially affect the effectiveness of the product (Soni et al., 2010; Oliveira et al., 2014).

Concluding Remarks

Listeria monocytogenes is a microorganism that occurs ubiquitously in nature and can be constantly reintroduced in food processing facilities. Good sanitization procedures are crucial to eliminate L. monocytogenes from food processing environments and prevent bacterial adhesion and biofilm formation, which often result in cross-contamination to food. Listeriosis was recognized as a serious disease in the last decades, probably as a function of advances in medical diagnosis, but also due to the changes in food processing (for example, use of cold for food preservation) and eating habits (increasing consumption of RTE foods). Continuous surveillance is needed to understand L. monocytogenes contamination dynamics in Brazil, and development of an effective surveillance system and compulsory notification of listeriosis, to facilitate the outbreaks investigation in Brazil, will then be possible to design better strategies to control the pathogen in food processing environments and food, as well as monitor the emergence of antibiotic resistance.