Abstract
Listeria monocytogenes is a zoonotic food-borne pathogen that is associated with serious public health and economic implications. In animals, L. monocytogenes can be associated with clinical listeriosis, which is characterised by symptoms such as abortion, encephalitis and septicaemia. In human beings, listeriosis symptoms include encephalitis, septicaemia and meningitis. In addition, listeriosis may cause gastroenteric symptoms in human beings and still births or spontaneous abortions in pregnant women. In the last few years, a number of reported outbreaks and sporadic cases associated with consumption of contaminated meat and meat products with L. monocytogenes have increased in developing countries. A variety of virulence factors play a role in the pathogenicity of L. monocytogenes. This zoonotic pathogen can be diagnosed using both classical microbiological techniques and molecular-based methods. There is limited information about L. monocytogenes recovered from meat and meat products in African countries. This review strives to: (1) provide information on prevalence and control measures of L. monocytogenes along the meat value chain, (2) describe the epidemiology of L. monocytogenes (3) provide an overview of different methods for detection and typing of L. monocytogenes for epidemiological, regulatory and trading purposes and (4) discuss the pathogenicity, virulence traits and antimicrobial resistance profiles of L. monocytogenes.
Keyword: Listeria monocytogenes; meat and meat products; epidemiology; virulence factors; diagnosis; antimicrobial resistance.
Listeria species
Listeria species (spp.) are short Gram-positive rods (Nyarko & Donnelly 2015) that belong to the phylum Firmicutes, class Bacilli, order Bacillales (Jadhav 2015). The Listeria spp. are facultatively anaerobic, non-spore forming, about 0.5 µm in width and 1 µm – 1.5 µm in length (Wieczorek, Dmowska & Osek 2012) and belong taxonomically to the Clostridium-Bacillus-Lactobacillus sub-branch with Brochothrix thermosphacta (Schmid et al. 2014). Listeria spp. are generally motile because of peritrichous flagella at temperature range of 24 °C – 28 °C but non-motile above 30 °C (Indrawattana et al. 2011). These species are also catalase positive; however, exceptions have been reported (Cepeda et al. 2006). Listeria spp. are oxidase, urea and indole negative and hydrolyse aesculin (De Vasconcelos Byrne et al. 2016). Listeria spp. also have the ability to tolerate salt conditions (NaCl) up to 20% (weight/volume [w/v]) and grows in a pH range of 4.4–9.6 (Holch et al. 2013). The growth temperature for these species ranges from –0.4 °C to 45 °C, with an optimum growth temperature of 37 °C and can survive at relatively low water activities (aw < 0.90) (Liu 2006). These growth conditions contribute to their versatility to grow and survive under extreme environmental conditions posed at food-processing facilities and become a serious problem for food industry (Ducey et al. 2006).
The genus Listeria consists of 20 low guanine (G) + cytosine (C) (38%) content species, which includes L. monocytogenes, L. marthii, L. innocua, L. welshimeri, L. seeligeri, L. costaricensis, L. ivanovii, L. grayi, L. rocourtiae, L. fleischmannii, L. newyorkensis, L. weihenstephanensis, L. floridensis, L. aquatica, L. thailandensis, L. cornellensis, L. riparia, L. booriae, L. Goaensis and L. Grandensis (Den Bakker et al. 2010). This classification of Listeria spp. is based on different analysis assays including 16S ribosomal ribonucleic acid (rRNA), deoxyribonucleic acid (DNA) sequencing information and multilocus enzyme analysis. It has also been proved useful for surveillance and epidemiological purposes in outbreaks linked to food-borne listeriosis (Chasseignaux et al. 2001). Out of the species of Listeria identified thus far, only L. monocytogenes can cause infection in both humans and animals, whereas L. ivanovii is pathogenic to animals, predominantly in ruminants and has rarely been implicated with human infections (Gouin et al. 1994; Orsi, Bakker and Wiedmann 2011; Zhang, Jayarao & Knabel 2004). However, L. Seeligeri and L. welshimeri have been reported as agents of sporadic cases of human listeriosis (Gouin et al. 1994).
Listeria spp. are phenotypically very similar but can be differentiated by biochemical tests including haemolysis test, acid production from D-xylose, L-rhamnose, mannitol, motility and alpha methy-D mannoside (Orsi et al. 2011). The Christie–Atkins–Munch-Peterson test can also be useful for differentiation of Listeria spp. This test works on the principle to test for haemolysis enhancement in the presence of Staphylococcus aureus (FDA et al. 2008).
Listeria spp. are mostly environmental contaminants with primary habitation of soil. However, these species have also been found in water, sewage and decaying vegetation (Willaarts, Pardo & De la Mora 2013). Listeria spp. have been found in a variety of animals including ruminants, birds, marine life, insects, ticks and crustaceans (Van Vuuren 2001). These species have been isolated from 1% to 7% of intestinal content of healthy animals (Borucki & Call 2003); thus animals can serve as carriers. Human beings are also carriers of Listeria spp. as these were isolated from 5% to 10% of stools of healthy human adults and 1.3% of the younger people (Churchill, Lee & Hall 2006). As a result of their ubiquitous and resilient character, Listeria spp. have the capacity to enter the food supply chain and contaminate a wide variety of food products (Leong, Alvarez-Ordóñez & Jordan 2014).
Listeria monocytogenes
Listeria monocytogenes was first described by Hülphers in 1910 from the necrotic liver of a rabbit in Sweden and named Bacillus hepatis (Carvalho, Sousa & Cabanes 2014; Hülphers 1911). Murray isolated a similar bacterium in 1926 as a causative agent of an epizootic in rabbits and guinea pigs in research laboratories of Cambridge, United Kingdom, and named Bacterium monocytogenes (Lekkas 2016; Murray, Webb & Swann 1926; Rantsiou et al. 2008). A year later (1927), Pirie also isolated a bacterium corresponding to the description given by Hülphers and Murray from wild gerbils in South Africa (SA) (Jemal 2014; Mitchell, Pirie & Ingram 1927). The bacterium was named Listerellahepatolytica in honour of British surgeon, Lord Joseph Lister, the father of antisepsis (Gray & Killinger 1966). However, it was until 1940, that the present name, L. monocytogenes was recognised (Lamont & Sobel 2011).
Listeria monocytogenes was first isolated in humans by Nyfeldt in 1929, and in the same year Gill also described the illness in sheep called circling diseases caused by L. monocytogenes (Gill et al. 1937; Nyfeldt 1929). Listeria monocytogenes was then recognised as pathogen that caused sporadic human infections and was mainly associated with workers encountering diseased animals (Lamont & Sobel 2011). In the 1980s, after several outbreaks including Vacherin Mont d’Or in Switzerland in 1983–1987 and improperly pasteurised milk in the United States (US) in 1983, that was when interest for the pathogen amongst food manufacturers started to emerge (Klumpp & Loessner 2013; Lekkas 2016). Since then, L. monocytogenes outbreaks have been linked to consumption of contaminated foods, which include dairy products, meat products, seafood products and vegetables (Loman 2012; Ragon et al. 2008; Zuber et al. 2019).
Listeria monocytogenes is amongst the dangerous bacterial food-borne pathogens in the world, which cause severe human diseases (Maertens de Noordhout et al. 2014). This pathogen has been divided into 13 serotypes (½a, ½b, ½c, 3a, 3b, 3c, 4a, 4ab, 4b, 4c, 4d, 4e, 7) based on somatic and flagellar antigens (Dhama et al. 2015). These serotypes are further grouped into four genetic diversity lineages (I–IV). These lineages consist of specific serotypes; lineage I harbours serotypes ½b, 3b, 4b, 4d, 4e and 7. Serotypes ½b and 4b within lineage I encode listeriolysin S virulence factor, which is not present in other lineages (Orsi et al. 2011). Lineage II contains serotypes ½a, ½c, 3a and 3c and often harbours several plasmids that are resistant to heavy metals (Dhama et al. 2015). Serotypes 4b, ½a, 4a and 4c belong to lineage III and 4a, 4c and atypical 4b serotypes have been characterised as lineage IV isolates (Haase et al. 2014). Lineage III and IV serotypes are rarely isolated and have distinctive genetic and phenotypic characteristics but occur mostly in ruminants (Camargo, Woodward & Nero 2016).
Human listeriosis
Listeriosis is a zoonotic disease that is mainly acquired through consumption of contaminated food by L. monocytogenes (Hilliard et al. 2018). Other possible routes of contamination for humans include direct contact with infected animals and environments (Vázquez-Boland et al. 2001). Uncommon occurrence of listeriosis has also been reported in human beings in the form of endocarditis, hepatitis, myocarditis, arteritis, pneumonia, sinusitis, conjunctivitis, ophthalmitis and joint infections (Amato et al. 2017). The incidences of listeriosis are very low in general population, but it remains a major and deadly food-borne disease with hospitalisation rate of over 95% (Scallan et al. 2011). This disease occurs in specific segments of the population, which are the elderly, pregnant women, unborn babies and immunocompromised people such as those suffering from acquired immune deficiency syndrome (AIDS) or cancer or those who have undergone organ transplants (Maertens de Noordhout et al. 2014).
Listeriosis is characterised by a wide spectrum of infections, which are categorised into two forms, namely severe invasive listeriosis and non-invasive febrile gastroenteritis (Buchanan et al. 2017). Invasive listeriosis mostly occurs in immunocompromised individuals and manifests itself as sepsis, meningitis, endocarditis, encephalitis, meningoencephalitis, septicaemia and brain infection (Doganay 2003). The brain infection because of listeriosis in immunocompromised adults is responsible for 22% fatalities, whereas endocarditis occurs in 10% of adults (Mizuno et al. 2007). Pregnant woman have 17-fold increased risk of contracting invasive listeriosis, and this infection mostly occurs in the third trimester (Mateus et al. 2013). Listeriosis in pregnant women is generally associated with flu-like symptoms with or without gastrointestinal problem (Doganay 2003). However, the consequences of foetus or newborn infection are extremely severe, which includes abortion, premature birth, pneumonia and meningitis (Indrawattana et al. 2011). Invasive listeriosis is responsible for over 90% of hospitalisation and between 20% and 30% case fatality rate (Leong et al. 2014), making it one of the most serious food-borne diseases.
Non-invasive gastroenteritis can manifest in immunocompetent adults and usually causes atypical meningitis, septicaemia and febrile gastroenteritis characterised by fever and watery diarrhoea lasting for 2–3 days, which is often accompanied by headache and backache (Mateus et al. 2013). These symptoms are usually self-limiting and can be resolved within a short period without seeking any medical attention, subsequently leading to undiagnosed and under reporting of cases (Matle 2016). In addition, the health workers are unlikely to report condition associated with non-invasive listeriosis because of their less severe manifestation when individuals seek medical attention. This poses a challenge to the health care system to maintain the knowledge and diagnose listeriosis cases especially in the developing world (Maertens de Noordhout et al. 2014).
The expression of both forms of listeriosis depends on the age of the individual, immune status of the individual, infectious dose and mode of infection, virulence of strain ingested and physiological stage (Poimenidou et al. 2018). The clinical signs of this disease often appear after a long incubation time (1 day – 70 days), which make epidemiological source tracing very difficult (Buchanan et al. 2017). Goulet et al. (2008) reported that incubation periods are largely influenced by clinical forms of the disease, with the longest incubation periods observed in pregnancy cases (median 27.5 days), followed by the central nervous system infection (median 9 days), sepsis (median 2 days) and febrile gastrointestinal disease (median 24 h). The estimated infective dose for listeriosis to occur in susceptible population is 0.1 to 10 million colony-forming units (cfu), whereas in healthy individual it is 10 to 100 million cfu (Angelo et al. 2017).
A study performed by Nappi et al. (2005) indicated that molecular characterisation of L. monocytogenes using serotyping allowed for the identification of the serotypes ½a, ½b and 4b as the predominate causative agents of listeriosis in humans. Furthermore, several studies showed that most human listeriosis outbreaks have been associated with L. monocytogenes serotype 4b, suggesting specific virulence properties in this serotype (De Cesare et al. 2001; Salcedo et al. 2003; Vasconcelos et al. 2008). Serotyping of L. monocytogenes isolates have also shown that serotypes belonging to antigenic group ½ (½a, ½b, ½c) have been over-represented in food isolates with sharp increase in clinical human isolates (Vázquez-Boland et al. 2001). No association have been established between certain forms of listeriosis and specific serotypes, but studies suggest a link between perinatal listeriosis and serotypes ½a and 4b (Soni et al. 2014). In Europe and North America, most human listeriosis cases over the past 20 years (2000–2010) involved serotype 4b and it was shown to be over-represented in perinatal listeriosis (Lacroix et al. 2014).
The four defined lineages (I, II, III and IV) of the L. monocytogenes, lineage I and II isolates have been associated with the majority of human listeriosis outbreaks and concurrent sporadic cases in the world (Schmitz-Esser et al. 2015). This suggests that serotypes harboured by these lineages have an increased virulence or a better adaptation to the human host (Corde et al. 2018). The distribution of these lineages varies by region with lineage II isolates mostly common amongst human listeriosis cases in Europe (Martín et al. 2014), compared with the US where lineage I strains seem to be predominant amongst human listeriosis cases (Roberts et al. 2018). The difference in geographical distribution of these lineages is linked to epidemic clones (ECs). Epidemic clones are closely related strains, associated with several geographically and temporally distinct listeriosis outbreaks (Chen & Knabel 2007). These ECs are also implicated in many human listeriosis outbreaks and contribute significantly to sporadic cases worldwide (Scortti et al. 2018). The ECI and ECII were each responsible for repeated human listeriosis in the US and Europe (Mammina et al. 2013). The ECIII caused a multistate outbreak associated with contaminated turkey (Chen & Knabel 2007).
Many food-borne listeriosis outbreaks have been linked to diverse food products, but different types of meat have been implicated in major human listeriosis outbreaks worldwide. Table 1 gives an overview of the listeriosis outbreaks associated with meat products during 1987–2018. The first laboratory-confirmed invasive case of listeriosis associated with meat products occurred in 1988 because of consumption of contaminated turkey franks (Schwartz et al. 2018). Since then, the vast majority of meat products were involved in listeriosis outbreaks or sporadic cases and included processed, vacuum-packaged meat products (Cases et al. 2016; Chen et al. 2017), pork tongue (Bozzuto, Ruggieri & Molinari 2010), sausages (Cases et al. 2016) and polony (Smith et al. 2019). The largest documented outbreaks of listeriosis in SA occurred between 2017 and 2018. This outbreak was associated with consumption of polony, which is a ready-to-eat (RTE) meat product and serotype 4b was the predominant isolate (Smith et al. 2019).
| TABLE 1: Major food-borne listeriosis outbreaks because of meat products in the world. |
Pathogenicity of Listeria monocytogenes
The success of L. monocytogenes to induce infection is because of the ability to promote its own internalisation through host cells (Carvalho et al. 2014). This pathogen has the capacity to pass three important barriers in the human host, namely the intestinal epithelium, the blood–brain barrier and the placenta and subsequently disseminate to other organs (Chen et al. 2009). The infection process of host cell by L. monocytogenes involved several different stages: adhesion and invasion of host cells, internalisation by host cells, lysis of vacuole, intracellular multiplication and intercellular spread to the adjacent cell (Vazquez-Boland et al. 2001). Upon ingestion through contaminated food, L. monocytogenes survives exposure to high acidity, bile salts, non-specific inflammatory attacks and proteolytic enzymes from the host system (Jeyaletchumi et al. 2012). Having survived this stage, L. monocytogenes adheres to and enters both phagocytic and non-phagocytic cells of the host through the assistance of surface proteins called internalin (Carvalho et al. 2014). The phagocyte cells possess mechanisms that are used to destroy ingested bacteria; therefore, the ability of L. monocytogenes to survive within these cells contributes to its pathogenicity (Wilson et al. 2018). After adhering to the epithelial tissue of the gastrointestinal tract through assistance of internalin proteins, L. monocytogenes is internalised by the macrophages in a primary phagosomal vacuole. After it has been internalised, L. monocytogenes escapes from phagosomal vacuole through the assistance of cytolysin called listeriolysin O (LLO) and phosphatidylinositol-specific phospholipase (plcA). The pathogen then replicates in the cytoplasm because of sufficient nutrients from the host. An actin-based motility machinery of the host cell facilitates intracellular movement of the organism across the cytoplasm to neighbouring cells (Neves et al. 2013), thus spreading the infection without re-exposure to host extracellular immune surveillance (Vazquez-Boland et al. 2001). Bacterial surface protein called actin polymerisation protein (ActA) was identified as the molecular determinant for intracellular movement of the L. monocytogenes within the cytoplasm (Bonazzi, Lecuit & Cossart 2009). Upon being internalised by neighbouring cells, L. monocytogenes is confined in a double-membrane vacuole from which it escapes with the assistance of LLO and plcB to restart its life cycle as has been shown in Figure 1.
 |
FIGURE 1: Pathogenesis and virulence genes involved in listeriosis infection in human cells. |
|
Virulence factors of Listeria monocytogenes
Listeria monocytogenes consists of a large group of virulence factors that contribute to its pathogenicity and act in various steps of host infection cycle (Jeyaletchumi et al. 2012). The majority of virulence determinants of L. monocytogenes are clustered along the chromosome in genomic islands or Listeria pathogenicity island-1 (LIPI-1) (Denes et al. 2014). However, LIPI-3 and LIPI-4 have also been identified through whole genome sequencings (WGSs) to carry important virulence factors of L. monocytogenes. The LIPI-1 contains six virulence factors, which include internalin (Hain et al. 2012), phosphatidylinositol-specific phospholipase (Gilmour et al. 2010), actin polymerisation protein and metalloprotease (encoded by mpl) (Jeyaletchumi et al. 2012). The expression of these genes is controlled by the positive regulatory factor A (PrfA) (Rabinovich et al. 2012).
Internalin
Adhesion and invasion of host cell by L. monocytogenes is the first step in intracellular life cycle. These steps are important for L. monocytogenes to cause disease in the host and are primarily mediated by two subfamilies of internalin proteins (Vazquez-Boland et al. 2001). The first subfamily is large surface proteins (70–80 kDa), such as inlA and inlB that attach to the bacterial cell through their C-terminal regions (Bonazzi et al. 2009). The second group is the smaller sized surface proteins (25 kDa – 30 kDa) such as inlC, inlD, inlE, inlF, inlG and inlH that lack the C-terminal cell-wall anchor region (Vazquez-Boland et al. 2001).
The adhesion of L. monocytogenes to the host and internalisation into a membrane bound vacuole is facilitated by inlA and inlB genes, which are encoded by inlAB operon (Hain et al. 2012; Hernandez-Milian & Payeras-Cifre 2014; Jeyaletchumi et al. 2012). The inlA is responsible for facilitating the binding between L. monocytogenes and the host adhesion protein E-cadherin for invasion of epithelial cells (Vazquez-Boland et al. 2001). An E-cadherin is a protein expressed on the surface of enterocytes (Lekkas 2016). This binding promotes local cytoskeletal rearrangements in the host cell to stimulate the uptake of L. monocytogenes by epithelial cells. The inlB binds the cellular receptor Met, a tyrosine kinase protein, which is also the endogenous ligand of the hepatocyte growth factor (Bonazzi et al. 2009). This binding allows L. monocytogenes to enter into a much wider range of host–cell types such as hepatocytes, fibroblasts and epithelioid cells (Sabet et al. 2005). The differences in expression of inlA and inlB are associated with poor invasion (Werbrouck et al. 2006) and mutations in inlA, which results in low invasion ability (Cases et al. 2016).
Other proteins of the internalin family include inlC and inlJ that are involved in post-intestinal dissemination of L. monocytogenes infection (Pournajaf et al. 2016). An InlC is produced after the L. monocytogenes has entered the host cell and functions to interact with IkB kinase (IKKα), which in turn prevents activation of nuclear factor-κB (NF-κB), a proinflammatory pathway (Liu et al. 2007) to dampen the host’s innate responses (Cases et al. 2016). An InlJ protein was discovered, as proteins that assist L. monocytogenes to cross the intestinal barrier of the host cell (Cases et al. 2016).
Listeriolysin O and phospholipases
Once L. monocytogenes invades the host cell, it is trapped in the single-layer membrane vacuole. However, later in the infectious process, the bacteria are surrounded by a double-membrane vacuole (Yu et al. 2018). Escaping from both layers of vacuole membranes is important for an effective infection, and failure to escape the membrane results in an infection that is removed fast from the tissues (Pushkareva & Ermolaeva 2010). The haemolysin (hly), gene, is responsible for producing a pore-forming surface toxin called LLO, which is required for lysis of vacuole membranes and the release of L. monocytogenes into cytoplasm (Kyoui et al. 2014). The absence of LLO equals avirulent strains of L. monocytogenes as the bacterium will not reach the cytoplasm (Pushkareva & Ermolaeva 2010); thus, it can be said that LLO is secreted by all virulent strains of L. monocytogenes. The LLO is highly affected by the environmental pH with higher levels of expression observed under acidic pH levels (pH < 6) and lower activity levels observed at neutral pH (Pushkareva & Ermolaeva 2010).
Listeriolysin S is another virulence factor that was identified by Cotter et al. (2008). This virulence factor is located in LIPI3 and it is regarded as secondary haemolysin, which is specifically found only on lineage I strains of L. monocytogenes. This second haemolysin is only induced under oxidative stress conditions, contributes to virulence of the pathogen as assessed by murine (mice and rats) and human polymorphonuclear neutrophil-based studies and is similar to the peptide streptolysin S produced by Streptococcus (Cotter et al. 2008).
Listeria monocytogenes also secretes phosphatidylinositol phospholipase C that are involved in the lysis of vacuole membranes. Two phospholipases that assist in lysis of vacuole membranes are plcA (Gouin et al. 1994) and plcB (Vazquez-Boland et al. 2001). Studies have showed that plcA assists in the escape of L. monocytogenes from the primary vacuole, whereas plcB is active during cell-to-cell spread of the bacteria (Doyle et al. 2013). Maturation of plcB is dependent on a zinc metalloprotease, which is encoded by mpl gene. Metalloprotease also assists hly, plcB and plcA to disrupt the primary vacuoles after host cell invasion (O’Connor et al. 2010).
Actin polymerising protein
Listeria monocytogenes reaches the cytoplasm after lyses of the vacuole and subsequently moves to infect other cells (Chatterjee et al. 2006). It achieves this by a surface protein called ActA that induces polymerisation of globular actin molecules to actin filaments. The filaments then facilitate movement of L. monocytogenes both inter- and intra-cellularly (Klumpp & Loessner 2013). Therefore, ActA is also required for L. monocytogenes pathogenicity (Vázquez-Boland et al. 2001), as it is critical in cytoplasmic movement of this pathogen. In a study performed by Doyle et al. (2013), using mice to compare the virulence of L. monocytogenes serotypes, the researchers observed lower virulence in serotypes 4a, 4c, 4d and 4e. The lower virulence in those serotypes was attributed to the production of lower levels of the ActA protein with actin tail formation. Serotypes 4a, 4c, 4d and 4e are considered avirulent strains because of lack of lower levels of ActA protein (Doyle et al. 2013).
Invasion-associated protein (Protein p60)
The invasion-associated protein (iap) is an extracellular protein p60 that is encoded by iap gene (Camejo et al. 2011). Protein p60 is common amongst Listeria spp. and regarded as an essential murine hydrolase enzyme that facilitates septum separation during the final stage of cell division (Yu et al. 2018). It is also involved in adherence of L. monocytogenes to the host cell and plays an important role in virulence and pathogenicity of this bacterium (Quendera et al. 2016).
Positive regulatory factor A
Expression of prfA is controlled in different ways either by PrfA itself or by an alternative sigma factor σB (Duroux et al. 2015). The temperature has an influence on the production of virulence factors because the secondary structure of untranslated prfA-mRNA is temperature dependent (Revazishvili et al. 2004). At 30 °C, the Shine-Dalgarno sequence is blocked and the ribosomes are not able to bind and translate the sequence. As a result of the positive feedback mechanism, only a small amount of prfA is therefore transcribed (Duroux et al. 2015). At 37 °C, the secondary structure has changed, which results in translation of prfA-mRNA followed by synthesis of PrfA and results in a higher amount of transcribed prfA. The prfA is the primary regulator of the expression of the virulence factors present in the virulence gene cluster (Figure 2), but other proteins act as virulence gene regulators too. The VirR is a response regulator critical for L. monocytogenes virulence (Ragon et al. 2008). The genes regulated by VirR encode ABC transporters, proteins involved in resistance to human defences in Staphylococcus aureus and cell wall modification proteins (Ragon et al. 2008). The alternative sigma factor σB is an overall regulator of the expression of several genes in response to several types of stresses, and it also regulates the expression of PrfA and thereby the expression of virulence factors. The PrfA is the primary regulator of the expression of the virulence factors present in the virulence gene cluster, but other proteins act as virulence gene regulators as well (Ryan et al. 2010).
 |
FIGURE 2: Organisation of the central virulence gene cluster of Listeria monocytogenes. |
|
Epidemiology of human listeriosis
The cases of human listeriosis and the number of high profile outbreaks that resulted in many deaths had significantly increased in many countries (De Castro et al. 2012). The increase is mainly because of changing consumption behaviours, as many individuals consume RTE foods (Mateus et al. 2013). Furthermore, globalisation of food trade and demographic changes such as increase in susceptible populations because of ageing and existence of other immune-compromising infections have augmented the risk of listeriosis (Wang et al. 2012). The introduction of sequencing methodologies for detection and typing of listeriosis outbreaks has also led to increased number of cases being reported (Zuber et al. 2019).
Epidemiological surveillance studies showed that human listeriosis is mostly reported in high-income and industrialised countries because of proper surveillance system for food-borne diseases (Grace 2015). Table 2 shows the overall incidence of listeriosis per 100 000 people in different developed countries. Surveillance of human listeriosis performed by European Union (EU) between 2006 and 2012 on 18 Member States reported a notification rate of 0.41 cases per 100 000 population (Food and Authority 2013). The highest notification rates were observed in Finland, Spain and Denmark with a hospitalisation rate of 91.6% on an average (Food and Authority 2013). The surveillance also reported an increased incidence of listeriosis in Greece (0.3), Sweden (0.6), Norwary (1.0), France (0.6) and Scandinavia (0.2). This trend is accounted for by increased cases in the population older than 60 years and the higher consumption of smoked fish in these countries (Food and Authority 2013). Furthermore, the surveillance reported 198 deaths because of listeriosis from 18 Member States. Furthermore, the EU performed wide baseline survey in 26 Member States between 2010 and 2011 to determine the prevalence of L. monocytogenes in food products at retail outlets (Food and Authority 2013). A total of 13 088 food samples including smoked or gravad fish (3053), meat products (3530) and cheese types (3452) were tested for the presence of L. monocytogenes. The EU prevalence of L. monocytogenes varied amongst different food products with the highest recorded in fish (10.4%), followed by meat products (2.07%) and cheese (0.47%) (Food and Authority 2013).
| TABLE 2: Incidences of listeriosis in different countries. |
The notification rate of human listeriosis in the US was reported to be approximately 0.3 cases per 100 000 population (Todd & Notermans 2011). This rate was similar to that reported in Canada and New Zealand, which was lower compared with Europe (Food and Authority 2013). In the US, approximately 1 600 individuals get listeriosis annually with 21% case fatality rate (Todd & Notermans 2011). Almost all the fatalities were reported in high-risk groups, such as older adults, pregnant women and people who were immunocompromised. The Foodborne Disease Active Surveillance Network (FoodNet) had a surveillance system in 10 states of America for laboratory-confirmed cases of food-borne diseases (Rip 2011). This system revealed that there is a greater likelihood of being hospitalised from illness caused by Listeria than any other food-borne pathogen in the US (Rip 2011).
The OzFoodNet which is a working group established by the Australian Government and Department of Health and Ageing to survey listeriosis reported an annual (2001–2010) incidence rate of 0.3 cases per 100 000 population in Australia (Popovic, Heron & Covacin 2014). According to the Japan Nosocomial Infections Surveillance, approximately 135–201 cases of human listeriosis occurred annually between 2008 and 2011 (Miya et al. 2015), which suggests an incidence rate that is equivalent to 1.40 cases per 100 000 populations. Cases of human listeriosis have also been reported in other Asian countries such as Taiwan that reported 48 cases of listeriosis between 1996 and 2018 (Laksanalamai et al. 2014), whereas China reported 479 cases over a period of 46 years (1964–2010) (Jadhav 2015).
The World Health Organization (WHO) evaluated the median rate of listeriosis in different regions in 2010 and estimated that the incidence of listeriosis in Africa was 0.1 cases per 100 000 populations (Carp-Cǎrare, Vlad-Sabie & Floriştean 2013). However, the data in this evaluation were limited as many African countries neither report nor monitor the incidence of listeriosis because of lack or absence of targeted surveillance programmes and reporting systems (Grace 2015; Todd & Notermans 2011). Despite the poor surveillance programmes and lack of epidemiological data to establish a comprehensive incidence rate of human listeriosis in Africa, there are a number of studies that reported the occurrence of L. monocytogenes in foods from African countries (Table 3) (Bouayad & Hamdi 2012; Derra et al. 2013; El-Shenawy et al. 2011; Matle et al. 2019).
| TABLE 3: Prevalence of Listeria monocytogenes in foods in Africa. |
In SA, an average of 60 to 80 laboratory-confirmed listeriosis cases were reported annually before 2017 (Smith et al. 2019). This suggests an incidence rate of 0.1 cases per 100 000 populations, which is in agreement with that reported by WHO. However, in 2017, an increase in laboratory-confirmed cases of listeriosis was reported by National Institute for Communicable Diseases (NICD), which was linked to an outbreak. In 2018, the NICD had identified a total of 1024 laboratory-confirmed human cases across all nine provinces of SA that resulted in 216 deaths. The majority of cases were reported in the Gauteng province (59%) followed by the Western Cape (13%) and KwaZulu-Natal (7%) provinces. These cases were mostly reported in vulnerable groups, which includes infants (≤ 28 days), HIV-positive individuals, the elderly (> 65 years) and pregnant mothers (Smith et al. 2019).
The Agricultural Research Council of SA performed a comprehensive national baseline survey across nine provinces of SA including major ports of entry between 2014 and 2016 to determine the occurrence of L. monocytogenes in meat and meat products in abattoirs, meat-processing plants and retail outlets. Meat samples (n = 2017) consisting of raw meat, processed meat and RTE meat were analysed for L. monocytogenes. The occurrence of L. monocytogenes in meat destined for the South African market varied between imported (12.4%) and domestic (15.0%) meat samples, with the highest proportion reported in processed meat (19.5%), followed by RTE (13.5%) meat products and raw (10.1%) meat (Matle et al. 2019).
Legislations relating to Listeria monocytogenes in food
Food-borne pathogens including L. monocytogenes remain a serious threat to public health and a significant impediment to socio-economic development worldwide (Grace 2015). Many countries responded to the threat posed by food-borne pathogens through implementation of strict regulations for microbiological standards or criteria in relation to contamination of food products (Strydom 2015). Microbiological criteria for food safety refer to the guidelines that are used to determine if a food product(s) is/are acceptable for human consumption based on the bacterial load of specific micro-organism on the food. The microbiological standards vary amongst different countries; however, they are guided by international standards such as International Commission on Microbiological Specifications for Food (ICMSF) and Codex Alimentarius Commission (CAC) (Rip 2011).
The ICMSF is a voluntary advisory organisation, which sets standards and methods regarding the presence of micro-organisms in food. The ICMSF states that food sample testing can be used for evaluation of safety and quality of food and to assess, validate the efficacy of microbial control measure such as Hazard Analysis and Critical Control Point (Rip 2011). The ICMSF recommends maximum of 100 cfu/g of L. monocytogenes in food at the time of consumption for non-risk consumers.
The CAC is a set of food standards, guidelines and codes of practice produced with the aim of protecting consumer health and facilitating international trade (Rip 2011). Compliance with the CAC standards is voluntary, but many governments and non-government institutions use the CAC guidelines as the basis for legislation and microbiological standards. The CAC standard on L. monocytogenes applies to only RTE foods, which divides them into three categories based on the ability of food product to support the growth of this pathogen (Food and Authority 2013). Microbiological criterion for L. monocytogenes in RTE foods belonging to the first category does not need to be determined. Therefore, microbiological criteria according to CAC have been set for RTE food products belonging to the second and third categories. The second group represents RTE foods that do not support the growth of L. monocytogenes, whereas the third group applies to the products that can support the growth of this pathogen. The acceptable level of 100 cfu/g has been set for food in the second category, whereas zero tolerance policy (absence of L. monocytogenes in 25 g of food) for products in the third category (Obaidat, Salman & Lafi 2015).
The European microbiological standard for L. monocytogenes in RTE food products is in accordance with CAC recommendations (Food and Authority 2013). The standard requires the absence of L. monocytogenes in RTE food products that are intended for infant consumption or as a medical food and in the food that can support the growth of this pathogen. However, in RTE food products that cannot support the growth of L. monocytogenes, the level < 100 cfu/g is required during the shelf life of those foods. Canada, Australia and New Zealand adopted microbiological standards similar to those of Europe as recommended by CAC (Jadhav 2015). The US has zero tolerance policy for L. monocytogenes in RTE food products and food-processing facilities and failure to comply is considered a serious offence (Piet et al. 2016).
In SA, meat safety is an important part of public health linking agriculture to health. The responsibility of ensuring meat safety is shared by two main national departments, namely the Department of Agriculture, Forestry & Fisheries (DAFF) and the Department of Health (DoH). The DAFF exercises authority over farms, feedlots and abattoirs and is mandated to administer the Animal Diseases Act, Act 35 of 1984 and the Meat Safety Act, Act 40 of 2000 (Magwedere, Songabe & Dziva 2015). As soon as the meat leaves the abattoir supervision of distribution, retail and marketing falls in the hands of the DoH, which is entrusted with the Foodstuffs, Cosmetics and Disinfectants Act (FCDA), Act 54 of 1972 (as amended by Act 39 of 2007). Section 2 (b) (i) of the FCDA does not allow any individual at food premises registered under this act to handle meat from an animal slaughtered in contravention of the Meat Safety Act. The FCDA forbids selling, manufacturing or importing for sale, any foodstuff that is contaminated, tainted or decayed or is in terms of any regulation deemed to be, detrimental to human health. However, these regulations are salient on microbiological criterion for L. monocytogenes in meat (Magwedere et al. 2015). The only microbiological criterion available for testing of meat in SA is the South Africa National Standard (SANS): 885:2011, which is non-mandatory and allows a maximum of 100 cfu/g for L. monocytogenes in RTE processed meat products.
Occurrence of Listeria monocytogenes in meat value chain
Listeria monocytogenes has been isolated from many different environments such as agricultural soil and vegetation (Susana et al. 2017), food-processing facilities (Martín et al. 2014) and retail outlets (Henri et al. 2016). Therefore, several sources have been identified as possible routes for contamination of food and subsequently transmission of L. monocytogenes to human beings. Contamination of meat and meat products with L. monocytogenes is a complex process that links primary food production (farm, feedlots) to retail outlets (Figure 3).
 |
FIGURE 3: Implicated routes of transmission for Listeria monocytogenes infection to humans. |
|
Listeria monocytogenes in animal farm
In the farm or feedlots, L. monocytogenes is mostly found in soil as natural inhabitant but often at relatively low numbers (O’Connor et al. 2010). Listeria monocytogenes can survive in the soil especially in agricultural soil for months and even grow (Rip 2011). Sauders et al. (2012) reported a prevalence range from 8.7% to 51.4% for L. monocytogenes in agricultural soil, whereas in non-agricultural soils the prevalence ranged between 15.2% and 43.2%. This suggests that the soil serves as the principal reservoir of L. Monocytogenes, where meat-producing animals are exposed to this pathogen through interaction with the natural environment. Contaminated soil dust has also been found to contain this pathogen, suggesting that the animal can acquire L. monocytogenes through air and subsequently transmit it to human beings through the meat value chain (Korthals et al. 2008).
Several studies have associated animal listeriosis with consumption of contaminated silage by L. Monocytogenes (Korthals et al. 2008; Harakeh et al. 2009; Parihar 2004; Werbrouck et al. 2006). Silages are a traditional feed used to conserve animals during forage shortage because of seasonal changes in dry season (Zhu, Gooneratne & Hussain 2017). Therefore, a poorly prepared silage can support the growth of L. monocytogenes that can subsequently infect animals (Nightingale et al. 2004). Faeces shed by infected animals along with silage are vehicles for primary infection in ruminants and reintroducing of L. monocytogenes into the environment (Lekkas 2016). Asymptomatic shedding of L. monocytogenes by infected animals can also transmit this pathogen to human beings through food (Piet et al. 2016). Other sources of L. monocytogenes in a farm include poor animal husbandry, natural water and wastewater source. Linke et al. (2014) found that natural water and wastewater sources near farming communities harbour large quantities of L. monocytogenes and may serve as sources of animal contamination.
As L. monocytogenes is found naturally in the environment, pathogen control measures should therefore start from farm level up until the meat reaches the consumers’ table. Pre-harvest pathogen control includes all measures and management practices at farm level to reduce the probability of having pathogens in animals and final meat products (Nørrung & Buncic 2008). This should aim to minimise sources, access, levels and transfer of contaminants to the animal. Technologies used to reduce pathogen levels in animals include diet manipulation (supplements), effective biosecurity and optimum animal welfare (Sofos & Geornaras 2010). Proper animal management practices such as provision of clean water and feed and proper waste management to limit spreading of pathogens into the environment also help to reduce pathogen levels in animals (Buncic et al. 2014). However, it is difficult for farmers to control pathogens at this level because of lack of knowledge, resources and money in some cases.
Listeria monocytogenes in food-processing facilities
Listeria monocytogenes has also been reported in different meat-processing facilities such as abattoirs, meat-processing plants and butcheries (Carpentier & Cerf 2011). Several studies suggest that animals presented for slaughter are an important source of initial contamination of meat-processing facilities with L. monocytogenes (Autio et al. 2000; Churchill et al. 2006; Lekkas 2016; Nigtingale et al. 2004). Autio et al. (2000) characterised different L. monocytogenes strains isolated from environmental samples in a pig farm and carcasses at abattoirs using pulsed-field gel electrophoresis (PFGE). The same pulsotypes were detected in a pig farm and carcasses, indicating that L. monocytogenes from farm might have contaminated the carcasses during production and processing cycle. Furthermore, Nel, Van Vuuren and Swan (2004) indicated that animals presented for slaughter often harbour large quantities of micro-organisms including L. monocytogenes on the external surface and hooves, which can be introduced in processing facilities if proper hygiene measures are not followed. In addition to animals, contamination may also enter the meat-processing facility through raw material and personnel carrying L. monocytogenes (El-Shenawy et al. 2011; Pava-Ripoll et al. 2012; Thévenot, Dernburg & Vernozy-Rozand 2006). Floors, floor drains, racks and rollers are also reported to be sources of contamination in meat-processing facilities (Thévenot et al. 2006).
Once L. monocytogenes enters the processing facilities it is unlikely to be eradicated if proper monitoring programmes are not intensive as its survival is influenced by several complex factors (Carpentier & Cerf 2011). The contributing factors to survival of L. monocytogenes include the ability to proliferate under harsh stress conditions such as low temperature, pH and osmotic stress (Takahashi et al. 2014), resistance to sanitation agents and formation of biofilms (Carpentier & Cerf 2011). Meat-processing facilities use cold storage (4 °C) to reduce the proliferation of bacteria on meat. Although this process is effective against many bacteria, it supports the growth of L. monocytogenes as this bacterium has the ability to survive at low temperature. The presence of cold shock proteins and sigma factor σB, encoded by sigB, in Listeria spp., help them to survive in low temperature and osmotic pressure (Leong et al. 2014).
The occurrence of L. monocytogenes in meat-processing environment may also increase or decrease because of sanitation (Carpentier & Cerf 2011). Sanitation is a process that consists of cleaning protocols, followed by disinfection. Proper cleaning and sanitation procedures decrease the occurrence of L. monocytogenes in a meat-processing facility. However, this pathogen is often found even after cleaning. It shows the persistence of some strains and, on many occasions, the insufficiency of the cleaning (Cruz & Fletcher 2011). During the cleaning process, detergents are used to remove microbial agent on food-processing areas. However, this process is hampered by the presence of harbourage sites within the facility and concentration of sanitation (Lourenço, Neves & Brito 2009). Harbourage sites are areas where the sanitation agents do not reach correctly, and as a result of this it allows the proliferation of L. monocytogenes. Several studies showed that L. monocytogenes has the ability to resist commonly used sanitation agents in food-processing facilities (Bremer, Monk & Butler 2002; Fouladynezhad et al. 2013; Pan et al. 2006). These studies also reported that the resistance of L. monocytogenes to sanitising agents in food-processing facilities is because of the formation of biofilms and they subsequently persist in facility for several years. In fact, these studies showed that L. monocytogenes could form biofilms on surfaces such as polyethylene, polyvinyl chloride, glass and stainless steel in food-processing facilities. The formation of biofilms are influenced by characteristics of strains, physical and chemical properties of the substrate for attachment, growth phase of the bacteria, temperature, growth media and the presence of other microorganisms (Carpentier & Cerf 2011).
Listeria monocytogenes in retail level
The detection of L. monocytogenes in meat and meat products at retail level does not mean that contamination occurred in the retail environment (Sauders et al. 2016). However, cross-contamination from surfaces, equipment and workers and persistence of strains have been identified as the main source of L. monocytogenes in retail products. Gombas et al. (2003) reported that meat products handled, sliced and packaged at retail outlets have high levels of L. monocytogenes than in products pre-packed at the abattoir. However, this depends on the level of hygienic practice followed by food handlers. Personal hygiene of meat handlers and proper sanitisation of contact surfaces and utensils are important to prevent cross-contamination or recontamination in retail outlets (Bogere & Baluka 2014). Storage temperatures should also be controlled to inhibit multiplication, surviving and growth of existing pathogens.
Listeria monocytogenes in meat and meat products
Several studies have reported the existence of L. monocytogenes in meat and meat products originating from different animal species including game (Lambertz et al. 2012; Kramarenko et al. 2013; WHO & World Organisation for Animal Health 2014). In a study performed by Vitas and Garcia-Jalon (2004) in Spain that examined 396 meat product samples collected from 55 small meat-processing units identified L. monocytogenes in 34.9% of minced pork and beef meat products and in 36.1% of poultry meat. In Sweden, a survey of 507 heat-treated RTE meat product samples from 110 municipalities were analysed for L. monocytogenes. This pathogen was detected in 61% of heat-treated ham meat products, followed by 12% of turkey, 9% of roast beef and 7% of sausage (Lambertz et al. 2012). In Estonia, a survey baseline conducted over 10 years (2008–2010) indicated that L. monocytogenes was prevalent in 18.7% of raw meat and raw meat products, and 2% in RTE meat products collected from various food-processing facilities (Kramarenko et al. 2013). In Ireland, RTE meat samples analysed between 2013 and 2014 identified L. monocytogenes in 4.2% of meat products collected from poultry (Leong et al. 2014). Ismaiel, Ali and Enan (2014) reported L. monocytogenes in beef carcasses, raw lean beef, frozen chicken meat and Camel meat. Dhanashree et al. (2003) and Okutani et al. (2004) isolated L. monocytogenes in various meat products in India and Japan, respectively. Matle et al. (2019) reported L. monocytogenes in various meat and meat products including raw intact meat (10.1%), raw processed meat (19.5%) and RTE meat products (13.5%) collected from cattle, pork, sheep, game and poultry in SA.
Diagnosis of Listeria monocytogenes
Identification of L. monocytogenes is extremely important for prevention and disease control. The method used for detection and isolation of L. monocytogenes has evolved over the years from cold enrichment technique to conventional and molecular methods (WHO & World Organisation for Animal Health 2014).
Conventional methods
Several conventional methods have been developed for isolation and identification of L. monocytogenes in food samples. The conventional method of isolation of L. monocytogenes includes antibody-based tests, enzyme-linked immunosorbent assay, culture-based methods and immune-capture techniques (Välimaa, Tilsala-Timisjärvi & Virtanen 2015). Out of these methods, culture-based tests are usually preferred for many reasons such as being sensitive, cheap and they remain the ‘gold standards’ compared with other methods that are validated (Barajas et al. 2019). In addition, pure colonies of the targeted organisms obtained by culture-based assays are useful for epidemiological surveillance and outbreak management purposes (WHO & World Organisation for Animal Health 2014). The drawbacks of culture-based methods include low resolution regarding distinguishing bacterial strains. Furthermore, these methods are laborious (Leong et al. 2014) and phenotypic changes because of environmental selection, contaminating bacteria and atypical reactions by atypical strains can provide false-negative results (Välimaa et al. 2015).
The isolation and identification of L. monocytogenes using culture-based methods involve the use of selective agents and enrichment procedure. The purpose of the selective agents is to inhibit other competing microflora whilst the enrichment procedure allows the increase of L. monocytogenes to detectable levels and the recovery of injured or stressed cells (Chen et al. 2017). There are three commonly used culture-based methods (Figures 4–6) for isolation of L. monocytogenes in foods because of international regulations and requirements. These methods include the International Standard (ISO), the United States Department of Agriculture (USDA) and One-Broth Listeria method (Gasanov, Hughes & Hansbro 2005; Gómez et al. 2013; Zhang et al. 2004). Although these methods are internationally recommended and accepted for testing of a wide variety of food matrices, they must be used in accordance with their scope.
 |
FIGURE 4: The illustration of International Standard method. |
|
 |
FIGURE 5: The illustration of United States Department of Agriculture method. |
|
 |
FIGURE 6: The illustration of ONE-Broth method. |
|
The ISO 11290 standard is recommended for isolation of L. monocytogenes in a large variety of food and feed products as well as environmental samples (Liu et al. 2007). The USDA method is recommended for the detection of Listeria spp. in meat and poultry food products and environmental swabs (Jeyaletchumi et al. 2012). One Broth Listeria method that has been approved by the Association Française de Normalisation (AFNOR) is used for isolation of Listeria spp. from dairy food products, meat, seafood and vegetables (Gasanov et al. 2005).
All above-mentioned methods involve a series of primary and secondary enrichments of the samples in selective broth media. The ISO 11290 method utilises Half Fraser Broth and Fraser Broth for primary and secondary enrichment, respectively. The USDA method uses a two-step enrichment in University of Vermont media, whereas the One Broth Listeria method uses a one-step enrichment in Listeria broth, which takes 2 days to produce results as opposed to the 5 and 4 days needed by ISO and USDA methods, respectively (Leong et al. 2017). These enrichment media contain different selective agents including cycloheximide, colistin, cefotetan, fosfomycin, lithium chloride, nalidixic acid, acriflavine, phenylethanol, ceftazidime, polymyxin B and moxalactam (Jadhav 2015). These antibiotics inhibit mostly the growth of Gram-negative bacteria that are often present as competitors in food samples. The mechanism of inhibition varies amongst these antibiotics, which includes inhibition of protein synthesis (cycloheximide, fosfomycin and nalidixic acid), disruption of the outer cell membrane of bacteria (colistin) and beta-lactamase (cefotetan) amongst others.
Following primary and secondary enrichment, the broth is generally plated onto selective or differential media. The ISO 11290 recommends the use of Oxford and PALCAM agar for detection and isolation of L. monocytogenes. The USDA uses chromogenic media such as Agar Listeria Ottaviani and Agosti and RAPID-L. mono (Leong et al. 2017), whereas One Broth Listeria method requires the use of Listeria Brilliance green agar. These media are typically dependent on the β-glucosidase activity of Listeria, which cleaves the chromogenic substrate producing blue or green colonies. Lecithin present in the agar is hydrolysed by phospholipase enzyme synthesised only by L. monocytogenes, leading to the formation of opaque halos around their colonies (Jeyaletchumi et al. 2012). Presumptive listerial colonies on selective agar are confirmed by rapid tests and on biochemical properties such as Gram stain, catalase test, motility test, ability to produce haemolysis on blood agar plates, Christie–Atkins–Munch-Peterson test with Rhodococcusequi and Staphylococcus aureus and carbohydrate utilisation tests.
Molecular methods of detection
Polymerase chain reaction-based methods for detection of Listeria monocytogenes
• Conventional polymerase chain reaction
The polymerase chain reaction (PCR) method has been used extensively for the detection of L. monocytogenes. Conventional PCR targets the most common and specific genes of L. monocytogenes such as hly, inlA, inlB, iap, plcA, plcB, 16S and 23S rRNA genes and dth-18 delayed type hypersensitivity protein (Jadhav 2015). The conventional PCR techniques are used more frequently than cultural procedures as they are simple and can provide quick results (Jeyaletchumi et al. 2012). However, this PCR cannot distinguish between live or dead cells or viable but not culturable cells (Truter 2015), metabolically injured, stressed cells or reliably detect low levels of L. monocytogenes (Jadhav 2015). Therefore, a positive sample through conventional PCR does not necessarily mean that the organism is alive and in required concentrations, which makes that organism a public health risk (Quendera et al. 2016).
Multiplex polymerase chain reaction
Multiplex PCR is another PCR-based method, which allows the detection of multiple strains from the same species or multiple pathogens in a sample simultaneously (Chen et al. 2017). The detection specificity of this method depends on the specific binding of the primer pair to the target sequence of the micro-organism. Ryu et al. (2013) developed a multiplex PCR method that can distinguish between five different Listeria spp. including L. monocytogenes by targeting different genes for each species. Multiplex PCR can detect between 1 and 100 cfu/mL Listeria (Jadhav 2015); however, similar to conventional PCR it can overestimate the presence of the pathogen because it cannot distinguish between live and dead cells.
Real-time polymerase chain reaction
Real-time PCR differs from other PCR techniques because the amplicon is observed as it accumulates. The procedure monitors the accumulation of fluorescence levels, which in turn depend on the amount of the accumulated PCR product. The fluorescent molecule can be either a target-specific probe labelled with a fluorescent dye together with a quencher molecule or can be a non-specific DNA-binding dye. The method is highly sensitive, can detect and trace amounts of target DNA, can be automated and has the ability to quantify bacterial load without any post-PCR handling. However, its disadvantages are that primer dimers can show fluorescence, it is highly dependent on primer concentration and design and it requires stringent quality controls.
Subtyping of Listeria monocytogenes
Subtyping is a process that is used to discriminate amongst different bacterial strains that belong to the same species (Jeyaletchumi et al. 2012). Subtyping procedures are very useful for source identification and tracking of individual strains of L. monocytogenes that are involved in listeriosis outbreaks and to determine the population genetics, taxonomy and epidemiology of this pathogen (Doumith et al. 2004). There are many subtyping methods, which are broadly grouped as phenotypic and genotypic; however, not all will be discussed in detail in the current study, as they are not within the scope of this review. Those methods are listed in Table 4.
| TABLE 4: Advantages and disadvantages of subtyping techniques used for Listeria monocytogenes strains. |
Phenotypic subtyping methods
Serotyping: Serotyping is the first method used to differentiate L. monocytogenes strains from each other based on antigen–antibodies reaction (Ntivuguruzwa 2016). Listeria monocytogenes serotyping is performed using the slide agglutination method that characterise L. monocytogenes into 13 serotypes (½a, ½b, ½c, 3a, 3b, 3c, 4a, 4ab, 4b, 4c, 4d, 4e and 7) using unique combinations from somatic (O) and flagellar (H) surface antigens (antisera) reaction (Doumith et al. 2004). The value of this method in epidemiological studies is very limited because of poor discriminative powers (Gasanov et al. 2005). Serotyping is also associated with many drawbacks including failure to provide consistent or reliable and repeatable results, and it measures the phenotypic characteristics of L. monocytogenes, which are often subjected to change and does not always accurately reflect the genotype of a micro-organism (Liu 2006). In addition, serotyping is time consuming, difficult and requires high-quality antisera (Shaker & Hassanien 2015). Antigen sharing between L. monocytogenes and L. Seeligeri may lead to detection of incorrect serotype (Liu 2006).
Genetic sub-typing methods
Polymerase chain reaction serogroup multiplex polymerase chain reaction assays: To overcome the limitations of slide agglutination and enzyme-linked immunosorbent assay (ELISA) serotyping, a multiplex PCR-based method was then introduced by Borucki and Call (2003) for serotyping L. monocytogenes into five PCR serogroups; IIa corresponded to serotypes ½a and 3a; IIc to ½c and 3c; IIb to ½b, 3b and 7; and IVb to 4b, 4d and 4e (Doumith et al. 2004). This method uses primer pairs that target five genes (lmo0737, lmo1118, ORF2110 and ORF2819 and prs) to characterise L. monocytogenes strains and assign those PCR serogroups (Doumith et al. 2004; Nho et al. 2015). However, this assay could not distinguish between ½a and 3a, ½c and 3c, ½b, 3b and 7, 4a and 4c and between 4b, 4d and 4e, but as 3a, 3c, 3b, 7, 4a, 4c, 4d and 4e are rarely involved in human listeriosis, this approach was considered to be suitable for rapid detection of serotypes. Although this method is quick, robust and easy to implement, it has limited discriminatory power, thus providing poor resolution for epidemiological typing (Nho et al. 2015).
Pulsed-field gel electrophoresis: The PFGE is considered as ‘gold standard’ subtyping method for source tracking and epidemiologic investigations of infection caused by L. monocytogenes. This is because of its high discrimination power, robustness and reproducibility (Martín et al. 2014). However, it is time consuming and labour intensive, usually taking 2–3 days to complete and requires equipment of relatively high cost (Li et al. 2017). In PFGE, the genomic DNA is digested (generally using AscI and ApaI enzymes) with infrequent cutting endonucleases, which results in the generation of fewer fragments with high molecular mass (Kalpana & Muriana 2002). These fragments can be separated on the basis of their size using PFGE (Ruppitsch et al. 2015). The PFGE usually separates DNA fragments of less than 50 kb, as DNA fragments above 50 kb produce large and diffused bands (Jersek et al. 1999). In addition, it uses electric fields of alternating direction, which cause the DNA fragments to continuously change direction. This results in the resolution of high molecular weight DNA into separate bands (Hopkins, Arnold & Threlfall 2007).
Multiple-locus variable number of tandem repeat analysis: The multiple-locus variable number of tandem repeat analysis (MLVA) works on the principle to detect variation in the number of tandem repeats (VNTRs) at a specific locus in the genome DNA. The VNTRs are short segments of DNA that have variable copy numbers that can be determined by performing PCR amplification. The size of the PCR product is then analysed on agarose gels and/or by DNA-sequencing systems. The PCR product sizes are then used to determine the number of repeats in each region (Volpe Sperry et al. 2008). Therefore, by combining the size differences from several repeat loci regions, a multidigit, strain-specific code (profile) can be acquired, and these profiles can therefore be used for cluster analysis (Møretrø, Langsrud and Heir 2013; Murphy et al. 2007). The MLVA gained acceptance as subtyping method of bacterial isolates because of its robustness, rapidness and high discriminatory power (Camargo et al. 2016). Many authors suggested that MLVA can be a useful tool for the characterisation of L. monocytogenes strains and that it represents an attractive first-line screening method to epidemiological investigations and listeriosis surveillance (Chenal-Francisque et al. 2015; Lindstedt et al. 2008; Murphy et al. 2007). However, the main drawback of MLVA is the lack of reproducibility and its results cannot be compared amongst different laboratories. In addition, VNTRs are unstable and can even undergo change during routine laboratory subculturing and therefore affect the reproducibility of the MLVA method.
Multilocus sequence typing: Different multilocus sequence typing (MLST) methods have been described for L. monocytogenes typing (Den Bakker et al. 2013; Roberts et al. 2018). The MLST depends on multiple gene fragments or genes to differentiate between subtypes (Jeyaletchumi et al. 2012). The method relies on amplification of seven loci from housekeeping genes that are analysed for nucleotide differences. This method has been shown to be more discriminatory when compared against the gold standard for typing of L. monocytogenes PFGE method (Leong et al. 2017). Furthermore, MLST is considered an expensive and time-consuming method because it requires numerous sequencing reactions per isolate and cannot be multiplexed and it does not have enough discriminatory power for 4b L. monocytogenes serotypes (Jadhav 2015), which are amongst the serotypes often implicated in outbreaks. Direct interrogation of single-nucleotide polymorphisms (SNPs) could offer a more efficient alternative for DNA sequence-based subtyping based on the fact that the majority of sites sequenced for MLST are invariant (Ducey et al. 2006).
Whole-genome sequencing: Despite the fact that the phenotypic and molecular methodologies mentioned above have numerous advantages, those techniques, however, give limited information about the pathogenic organism because of discriminatory capacity (Lekkas 2016). The WGS has the power to overcome this hurdle and group isolates into epidemiologically relevant groups. The WGS has been recommended as new gold standard for subtyping of L. monocytogenes strain associated with outbreak (Fox et al. 2016). This technique has greatly improved since its inception, with the reduction in process time and the introduction of high-throughput next-generation sequencing technology. Furthermore, the technology is becoming cheaper and more user-friendly. In addition to epidemiological data, WGS can provide rapid generation of whole-genome sequence data that can help to identify targets that could be used to develop assays (Lekkas 2016).
Although the use of WGS provides valuable information that was not available previously in such a short time period, there are still major barriers that need to be addressed before these techniques can be incorporated in food-borne pathogen detection (Lekkas 2016). The need for computer platforms that are operator friendly, powerful enough to handle the massive data bases that are created and are easily interpreted still exists. In addition, there is no consensus on how these data will be stored or used by regulatory authorities such as FDA and CDC during inspections or outbreak investigations. It is almost certain that within the volume of data collected there will be some sequence data that might be misconstrued as indicating a health hazard (Eruteya & Odunfa 2014). Furthermore, limitations of the WGS approach are the need for highly trained bioinformatics professionals that smaller companies will not be able to afford, lack of standardised and validated protocols like the ones already existing for PFGE, lack of reference databases and lastly a large investment of resources that also have their own limitations (Orsi et al. 2011). In addition, food-borne pathogens are usually found at very low numbers, which poses its own limitations for epidemiological studies (Lekkas 2016).
Treatment
Treatment of human listeriosis can be a challenging task as L. monocytogenes may invade almost all cell types (Dhama et al. 2015). Furthermore, the treatment of human listeriosis is often ineffective because of long incubation period of L. monocytogenes, which makes the treatment period to vary according to the level of the infection. However, antibiotics have been used to treat human listeriosis successfully for a very long time (Al-Nabulsi et al. 2015). Listeria monocytogenes is generally susceptible to the majority of antibiotics, but cephalosporin, fosfomycin and fluoroquinolones are not active against this pathogen (Noll, Kleta & Al 2018). The intrinsic resistance of L. monocytogenes against these antibiotics is because of lack or low affinity of enzyme catalysing the final step of cell wall synthesis (Al-Nabulsi et al. 2015). The antibiotic of choice for treating human listeriosis is ampicillin or penicillin G in combination with an aminoglycoside such as gentamicin. Trimethoprim in combination with a sulfonamide, such as sulfamethoxazole-co-trimoxazole, is considered second choice of therapy (Kovacevic et al. 2013). Furthermore, tetracycline, erythromycin and vancomycin have been used to treat human listeriosis (Rip 2011). However, evolution of bacteria towards resistance has been considerably accelerated in L. monocytogenes (Moreno et al. 2014).
Antimicrobial resistance in Listeria monocytogenes
The acceleration in antimicrobial resistance of L. monocytogenes is linked to selective pressure exerted by over-prescription of drugs in clinical settings and their heavy use as promoters for growth in farm animals and increased global trade and travel, which favour the spread of antimicrobial resistance between countries and continents (Moreno et al. 2014; Zhang et al. 2004). Resistant L. monocytogenes strains have been reported against first-line antibiotics. Gentamicin-resistant clinical strains of L. monocytogenes were reported (Walsh et al. 2001). Listeria monocytogenes strain resistant to ampicillin was identified in the US (Verraes et al. 2013). Listeria monocytogenes resistant to streptomycin, erythromycin, kanamycin, sulfonamide and rifampin were also reported in clinical isolates in different countries (Moreno et al. 2014; Zhang et al. 2004). Multiple drug resistance has also been observed in strains isolated from foods and environmental samples across the world (Morobe et al. 2009). A study conducted in Northern Ireland (Walsh et al. 2001) showed 0.6% of L. monocytogenes from retail foods. Furthermore, antimicrobial resistance of L. monocytogenes isolated from food and animal sources (n = 167) in the US was determined. The resistance to ciprofloxacin, tetracycline, sulfonamide and nalidixic acid were 1.8%, 9%, 73% and 100%, respectively (Zhang et al. 2004).
Mechanisms of antibiotic resistance in Listeria monocytogenes
Listeria monocytogenes becomes resistant to antimicrobial agents through acquisition of three types of movable genetic elements, namely self-transferable plasmids, mobilisable plasmids and conjugative transposons (Moreno et al. 2014). Efflux pumps were reported to be associated with fluoroquinolone resistance in Listeria (Wilson et al. 2018). However, there is an increase in reports of L. monocytogenes spontaneously acquiring resistant genes through mutations (Moreno et al. 2014). Mutations that occur in the promoter or operator coding regions can lead to overexpression of the endogenous genes such as those that encode for antimicrobial inactivating enzymes like the β-lactamase AmpCgene (Siu et al. 2003). Point mutations that occur in genes encoding for antimicrobial target regions can result in a target site that is resistant to the antimicrobial activity. Such a mutation was seen in the gyrase gene, whose mutation led to the expression of a fluoroquinolone-resistant gyrase enzyme (Hopkins et al. 2007).
Antibiotic resistance mediated by conjugation
Conjugation is the process of transfer of genetic material, which occurs between living bacterial cells that are in direct contact (Verraes et al. 2013). Conjugation is the major mechanism used by L. monocytogenes strains to acquire antimicrobial resistance. Enterococci and Streptococci, in particular, represent a reservoir of resistance genes for L. monocytogenes. The gastrointestinal tract of humans is considered the most probable site where the acquisition by Listeria spp. of conjugative plasmids and transposons from Enterococcus–Streptococcus takes place (Wilson et al. 2018).
Charpentier and Courvalin (1999) reported that a broad host-range of plasmid pIP510 and pAMß1 initially found in Streptococcus agalactiae and Enterococcus faecalis, respectively, encoding resistance to chloramphenicol, macrolides, lincosamides erythromycin and streptogramins can be transferred by conjugation to L. monocytogenes. The Tn916, a broad host-range conjugative transposon that is primarily found in Enterococcus faecalis can also be conjugated from E. faecalis to L. innocua (Walsh et al. 2001). Conjugative transfer of the Tn916-related transposon Tn1545, initially found in Streptococcus pneumoniae was obtained from E. faecalis to L. monocytogenes in vitro and in vivo (Mata, Baquero & Pe 2000). Conjugative plasmids and transposons originating from Enterococcus–Streptococcus responsible for the emergence of resistance to tetracycline and chloramphenicol in L. monocytogenes have been reported (Walsh et al. 2001).
Active efflux of antibiotics
Efflux mechanisms in L. monocytogenes was first reported in 2000 (Mata et al. 2000). The sequence of MdrL (multidrug efflux transporter of Listeria) protein is highly homological to the sequence of protein YfmO, a putative chromosomal multidrug efflux transporter of Bacillus subtilis. An allele-substituted mutant of this gene in L. monocytogenes failed to pump out ethidium bromide and presented increased susceptibility to macrolides, cefotaxime and heavy metals. Efflux pump Lde (Listeria drug efflux) is associated with fluoroquinolone resistance in clinical isolates of L. monocytogenes in France (Verraes et al. 2013). The Lde protein showed 44% homology with PmrA (pneumoniae multidrug resistance) of Streptococcus pneumoniae, which belongs to the major facilitator superfamily of secondary multidrug transporters. The insertional inactivation of the gene Lde resulted in increased susceptibility of fluoroquinolones in L. monocytogenes (Verraes et al. 2013).
Alternative methods to control Listeria monocytogenes
Different alternative methods and therapies have been explored to reduce the presence of L. monocytogenes in foods, as there are few therapeutic options because of rapid development of antimicrobial resistance in this pathogen. The use of bacteriophage as biocontrol for L. monocytogenes and bacteriocins and essential oils in food, food-processing plants and humans has been reported (Klumpp & Loessner 2013; Soni et al. 2014). The use of probiotics has also been reported to inhibit growth of L. monocytogenes as they enhanced host immunity (Dhama et al. 2015).
Bacteriophages are viruses that can kill bacteria and were found as candidates for biocontrol of L. monocytogenes in meat and meat products during processing and packaging (Strydom 2015). Bacteriophages showed a high degree of specificity to lysis of L. monocytogenes strains without detrimental effects on normal microflora of the ultimate consumer and other desired bacteria in the food (Dhama et al. 2015). Furthermore, bacteriophages can self-perpetuate and they are stable during long cold storage (Strydom 2015). This suggests bacteriophages will be active against L. monocytogenes post-processing. Based on these desirable attributes, several commercial bacteriophage-based products have been developed for biocontrol of L. monocytogenes in food (Leong et al. 2017), which includes Phage LM-103a, phage LMP-102a, (Strydom 2015), Ply511 phage, ListShield, ListexP-100 and ListexTM (Dhama et al. 2015). These products have been reported to function effectively against L. monocytogenes in foods and food facilities in different countries. For example, ListexP-100 and ListShield are used to control L. monocytogenes in the Netherlands and the US, respectively (Dhama et al. 2015). However, other countries such as SA still do not permit the use of bacteriophage-based products in food products and food-processing plants (Strydom 2015).
Bacteriocins are ribosomally synthesised antimicrobial peptides that can disrupt the integrity of the target cell membrane through forming pore on the membrane. The bacteriocins such as nisin have been used in meat products to inhibit the growth of L. monocytogenes (Rahimi et al. 2012). Bacteriocins have the potential to inhibit a wide variety of unrelated species or only closely related species. Recently nisin has been reported against L. monocytogenes and limited data have been generated to complete the understanding of the potential use for other bacteriocins for biocontrol of food-borne pathogens (Leong et al. 2017). Furthermore, essential oils from plant extracts have potential antimicrobial properties, which are suggested to reduce the survival of L. monocytogenes in various products. These essential oils include thyme, rosemary and oregano (Hilliard et al. 2018) and those from Cinnamomum cuspidatum and Cinnamomum crassinervium (Dhama et al. 2015).
Conclusion
Listeria monocytogenes is amongst major food-borne pathogen in the world that has commanded most research and surveillance attention from government agencies and food industry over the last few years. Furthermore, methods for isolation, detection, identification and subtyping for L. monocytogenes from food products have increased rapidly with WGS as the new gold standard for typing of this pathogen. Despite the extensive research and development on L. monocytogenes, outbreaks associated with this pathogen continue to be reported and are exacerbated by a high number of susceptible individuals in most countries. However, there are no data on prevalence of L. monocytogenes from most African countries that are considered to have a significant population that is immunocompromised because of HIV, TB, malaria and other infectious diseases associated with poverty. Therefore, targeted surveillance programmes are necessary in those countries not only to determine prevalence but also for the development of regulations and microbiological criterion. In addition, increases in antibiotic resistance amongst L. monocytogenes strains are in line with a worldwide pattern of an increasing prevalence of antibiotic resistance amongst food-borne pathogens. Alternative therapies such as bacteriophages, bacteriocins and essential oil have been explored and show promising results.
Acknowledgements
The following organisations and individuals are acknowledged for their contributions: Department of Agriculture, Land Reform and Rural Development – Directorate: Veterinary Public Health for project funding and the use of data for this study. The officials from the Department of Agriculture, Forestry, and Fisheries – Directorate: Veterinary Public Health (Lizzy Molele, Pauline Modibane, Maphaseka Mosia, Mavis Phaswane and Maruping Ntsatsi) for the field collection of samples for this study and Mphane Molefe for authorising funding allocation and the approval of the study. The authors are grateful to the Agricultural Research Council: Onderstepoort Veterinary Research for providing all research facilities.
Competing interests
The authors have declared that no competing interests exist.
Authors’ contributions
I.M. conceived part of the review and wrote the manuscript. K.R.M. supervised part of the project and reviewed the article. E.M. conceived the project, obtained funding for the project, designed the study, supervised sample collection and data capture and reviewed the article.
Funding information
The study was funded by the Department of Agriculture, Land Reform and Rural Development (DALRRD) under project number 21.1.1/VPH-01/OVI.
Ethical consideration
The authors confirm that ethical clearance was not required for the study.
Data availability statement
Data sharing is not applicable to this article as no new data were created or analysed in this study.
Disclaimer
The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of any affiliated agency of the authors.’
References
Al-Nabulsi, A.A., Osaili, T.M., Awad, A.A., Olaimat, A.N., Shaker, R.R. and Holley, R.A., 2015, ‘Occurrence and antibiotic susceptibility of Listeria monocytogenes isolated from raw and processed meat products in Amman, Jordan’, CyTA – Journal of Food, Vol. 13(3), 1–7. https://doi.org/10.1080/19476337.2014.982191
Amato, E., Filipello, V., Gori, M., Lomonaco, S., Losio, M.N., Parisi, A. et al., 2017, ‘Identification of a major Listeria monocytogenes outbreak clone linked to soft cheese in Northern Italy – 2009–2011’, BMC Infectious Diseases 17(1), 1–7. https://doi.org/10.1186/s12879-017-2441-6
Angelo, K.M., Conrad, A.R., Saupe, A., Dragoo, H., West, N., Sorenson, A. et al., 2017, ‘Multistate outbreak of Listeria monocytogenes infections linked to whole apples used in commercially produced, prepackaged caramel apples: United States, 2014–2015’, Epidemiology and Infection 145(05), 848–856. https://doi.org/10.1017/S0950268816003083
Autio, T., Säteri, T., Fredriksson-Ahomaa, M., Rahkio, M., Lundén, J. & Korkeala, H., 2000, ‘Listeria monocytogenes contamination pattern in pig slaughterhouses’, Journal of Food Protection 63(10), 1438–1442. https://doi.org/10.4315/0362-028X-63.10.1438
Barajas, H.R., Romero, M.F., Martínez-sánchez, S. & Alcaraz, L.D., 2019, ‘Global genomic similarity and core genome sequence diversity of the Streptococcus genus as a toolkit to identify closely related bacterial species in complex environments’, Peer J 6, e6233. https://doi.org/10.7717/peerj.6233
Bogere, P. & Baluka, A.S. (2014), ‘Microbiological quality of meat at the abattoir and butchery levels in Kampala City, Uganda’, Internet Journal of Food Safety 16(2014), 29–35.
Bonazzi, M., Lecuit, M. & Cossart, P., 2009, ‘Listeria monocytogenes internalin and E-cadherin: From bench to bedside’, Cold Spring Harbor Perspectives in Biology 1(4), a003087. https://doi.org/10.1101/cshperspect.a003087
Borucki, M.K. & Call, D.R., 2003, ‘Listeria monocytogenes serotype identification by PCR’, Journal of Clinical Microbiology 41(12), 5537–5540. https://doi.org/10.1128/JCM.41.12.5537-5540.2003
Bouayad, L. & Hamdi, T.M., 2012, ‘Prevalence of Listeria spp. in ready to eat foods (RTE) from Algiers (Algeria)’, Food Control 23(2), 397–399. https://doi.org/10.1016/j.foodcont.2011.08.006
Bozzuto, G., Ruggieri, P. & Molinari, A., 2010, ‘Molecular aspects of tumor cell migration and invasion’, Annali dell’Istituto superiore di sanità 46(1), 66–80. https://doi.org/10.4415/Ann_10_01_09
Bremer, P.J., Monk, I. & Butler, R., 2002, ‘Inactivation of Listeria monocytogenes/Flavobacterium spp. biofilms using chlorine: Impact of substrate, pH, time and concentration’, Letters in Applied Microbiology 35(4), 321–325. https://doi.org/10.1046/j.1472-765X.2002.01198.x
Buchanan, R.L., Gorris, L.G.M., Hayman, M.M., Jackson, T.C. & Whiting, R.C., 2018, ‘A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments’, Food Control 75, 1–13. https://doi.org/10.1016/j.foodcont.2016.12.016
Buncic, S., Nychas, G.J., Lee, M.R.F., Koutsoumanis, K., Hébraud, M., Desvaux, M. et al., 2014, ‘Microbial pathogen control in the beef chain: Recent research advances’, Meat Science 97(3), 288–297. https://doi.org/10.1016/j.meatsci.2013.04.040
Camargo, A.C., Woodward, J.J. & Nero, L.A., 2016, ‘The continuous challenge of characterizing the foodborne pathogen Listeria monocytogenes’, Foodborne Pathogens and Disease 13(8), 405–416. https://doi.org/10.1089/fpd.2015.2115
Camejo, A., Carvalho, F., Reis, O., Leitão, E., Sousa, S. & Cabanes, D., 2011, ‘The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle’, Virulence 2(5), 379–394. https://doi.org/10.4161/viru.2.5.17703
Carp-Cǎrare, C., Vlad-Sabie, A. & Floriştean, V.-C., 2013, ‘Detection and serotyping of Listeria monocytogenes in some food products from North-East of Romania’, Revista Romana de Medicina de Laborator 21(3–4), 285–292. https://doi.org/10.2478/rrlm-2013-0025
Carpentier, B. & Cerf, O., 2011, ‘Review – Persistence of Listeria monocytogenes in food industry equipment and premises’, International Journal of Food Microbiology 145(1), 1–8. https://doi.org/10.1016/j.ijfoodmicro.2011.01.005
Carvalho, F., Sousa, S. & Cabanes, D., 2014, ‘How Listeria monocytogenes organizes its surface for virulence’, Frontiers in Cellular and Infection Microbiology 4(48), 1–11. https://doi.org/10.3389/fcimb.2014.00048
Cases, L., Jensen, A.K., Björkman, J.T., Ethelberg, S., Kiil, K., Kemp, M. & Nielsen, E.M., 2016, ‘Molecular typing and epidemiology of human listeriosis cases, Denmark, 2002–2012’, Emerging Infectious Diseases 22(4), 62. https://doi.org/10.3201/eid2204.150998
Cepeda, J.A., Millar, M., Sheridan, E.A., Warwick, S., Raftery, M., Bean, D.C. et al., 2006, ‘Listeriosis due to infection with a catalase-negative strain of Listeria monocytogenes’, Journal of Clinical Microbiology 44(5), 1917–1918. https://doi.org/10.1128/JCM.44.5.1917-1918.2006
Charpentier, E. & Courvalin, P., 1999, ‘MINIREVIEW antibiotic resistance in Listeria spp.’, Antimicrobial Agents and Chemotherapy 43(9), 2103–2108. https://doi.org/10.1128/AAC.43.9.2103
Chasseignaux, E., Toquin, M., Ragimbeau, C., Salvat, G., Colin, P. & Ermel, G., 2001, ‘Molecular epidemiology of Listeria monocytogenes isolates collected from the environment, raw meat and raw products in two poultry- and pork-processing plants’, Journal of Applied Microbiology 91(5), 888–899. https://doi.org/10.1046/j.1365-2672.2001.01445.x
Chatterjee, S.S., Chatterjee, S.S., Hossain, H., Otten, S., Kuenne, C., Kuchmina, K. et al., 2006, ‘Intracellular gene expression profile of Listeria monocytogenes intracellular gene expression profile of listeria monocytogenes’, Infection and Immunity 74(2), 1323–1338. https://doi.org/10.1128/IAI.74.2.1323-1338.2006
Chen, J., Luo, X., Jiang, L., Jin, P., Wei, W., Liu, D. et al., 2009, ‘Molecular characteristics and virulence potential of Listeria monocytogenes isolates from Chinese food systems’, Food Microbiology 26(1), 103–111. https://doi.org/10.1016/j.fm.2008.08.003
Chen, J.-Q., Regan, P., Laksanalamai, P., Healey, S. & Hu, Z., 2017, ‘Prevalence and methodologies for detection, characterization and subtyping of Listeria monocytogenes and L. ivanovii in foods and environmental sources’, Food Science and Human Wellness 6(3), 97–120. https://doi.org/10.1016/j.fshw.2017.06.002
Chen, Y. & Knabel, S.J., 2007, ‘Multiplex PCR for simultaneous detection of bacteria of the genus Listeria,Listeria monocytogenes, and major serotypes and epidemic clones of L. monocytogenes’, Applied and Environmental Microbiology 73(19), 6299–6304. https://doi.org/10.1128/AEM.00961-07
Chenal-Francisque, V., Maury, M.M., Lavina, M., Touchon, M., Leclercq, A. & Lecuit, M., 2015, ‘Clonogrouping, a rapid multiplex pcr method for identification of major clones of Listeria monocytogenes’, Journal of Clinical Microbiology 53(10), 3355–3358. https://doi.org/10.1128/JCM.00738-15
Churchill, R.L.T., Lee, H. & Hall, J.C., 2006, ‘Detection of Listeria monocytogenes and the toxin listeriolysin O in food’, Journal of microbiological methods 64(2), 141–170. https://doi.org/10.1016/j.mimet.2005.10.007
Corde, Y., Teixeira, A.P., Kerouanton, A., Te, S., Mereghetti, L., Brisabois, A. et al., 2018, ‘BRIEF REPORT A Listeria monocytogenes strain is still virulent despite nonfunctional major virulence genes’, The Journal of Infectious Diseases 200(12), 1944–1948. https://doi.org/10.1086/648402
Cotter, P.D., Draper, L.A., Lawton, E.M., Daly, K.M., Groeger, D.S., Casey, P.G. et al., 2008, ‘Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes’, PLoS Pathogens 4(9), e1000144. https://doi.org/10.1371/journal.ppat.1000144
Cruz, C.D. & Fletcher, G.C., 2011, ‘Prevalence and biofilm-forming ability of Listeria monocytogenes in New Zealand mussel (Perna canaliculus) processing plants’, Food Microbiology 28(7), 1387–1393. https://doi.org/10.1016/j.fm.2011.06.014
De Castro, V., Escudero, J.M., Rodriguez, J.L., Muniozguren, N., Uribarri, J., Saez, D. et al., 2012, ‘Listeriosis outbreak caused by Latin-style fresh cheese’, Eurosurveillance 17(42), 3–5.
De Cesare, A., Bruce, J.L., Dambaugh, T.R., Guerzoni, M.E. & Wiedmann, M. (2001), ‘Automated ribotyping using different enzymes to improve discrimination of Listeria monocytogenes isolates, with a particular focus on serotype 4b strains’, Journal of Clinical Microbiology 39(8), 3002–3005. https://doi.org/10.1128/JCM.39.8.3002-3005.2001
De Vasconcelos Byrne, V., Hofer, E., Vallim, D.C. & De Castro Almeida, R.C., 2016, ‘Occurrence and antimicrobial resistance patterns of Listeria monocytogenes isolated from vegetables’, Brazilian Journal of Microbiology 47(2), 438–443. https://doi.org/10.1016/j.bjm.2015.11.033
Den Bakker, H.C., Cummings, C.A., Ferreira, V., Vatta, P., Orsi, R.H., Degoricija, L. et al., 2010, ‘Comparative genomics of the bacterial genus Listeria: Genome evolution is characterized by limited gene acquisition and limited gene loss’, BMC Genomics 11(1), 688. https://doi.org/10.1186/1471-2164-11-688
Den Bakker, H.C., Desjardins, C.A., Griggs, A.D., Peters, J.E., Zeng, Q., Young, S.K. et al. 2013, ‘Evolutionary dynamics of the accessory genome of Listeria monocytogenes’, PLoS One 8(6), e67511. https://doi.org/10.1371/journal.pone.0067511
Denes, T., Vongkamjan, K., Ackermann, H., Switt, I.M. & Wiedmann, M., 2014, ‘Comparative genomic and morphological analyses of Listeria phages isolated from farm environments’, Applied and Environmental Microbiology 80(15), 4616–4625. https://doi.org/10.1128/AEM.00720-14
Derra, F.A., Karlsmose, S., Monga, D.P., Mache, A., Svendsen, C.A., Félix, B. et al., 2013, ‘Occurrence of Listeria spp. in retail meat and dairy products in the area of Addis Ababa, Ethiopia’, Foodborne Pathogens and Disease 10(6), 577–579. https://doi.org/10.1089/fpd.2012.1361
Dhama, K., Karthik, K., Tiwari, R., Shabbir, Z., Barbuddhe, S., Veer, S. et al., 2015, ‘Listeriosis in animals, its public health significance (food-borne zoonosis) and advances in diagnosis and control: A comprehensive review’, Veterinary Quarterly 35(4), 211–235. https://doi.org/10.1080/01652176.2015.1063023
Dhanashree, B., Otta, S.K., Karunasagar, I. & Goebel, W., 2003, ‘Incidence of Listeria spp. in clinical and food samples in Mangalore, India’, Food Microbiology 20(4), 447–453. https://doi.org/10.1016/S0740-0020(02)00140-5
Djordjevic, D., Wiedmann, M. & Mclandsborough, L.A., 2002, ‘Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation’, Applied and Environmental Microbiology 68(6), 2950–2958. https://doi.org/10.1128/AEM.68.6.2950-2958.2002
Doganay, M., 2003, ‘Listeriosis: Clinical presentation’, FEMS Immunology & Medical Microbiology 35(3), 173–175. https://doi.org/10.1016/S0928-8244(02)00467-4
Doorduyn, Y., Van Den Brandhof, W.E., Van Duynhoven, Y.T.H.P., Wannet, W.J.B. & Van Pelt, W., 2006, ‘Risk factors for Salmonellaenteritidis and Typhimurium (DT104 and non-DT104) infections in The Netherlands: Predominant roles for raw eggs in Enteritidis and sandboxes in Typhimurium infections’, Epidemiology and Infection 134(3), 617–626. https://doi.org/10.1017/S0950268805005406
Doumith, M., Buchrieser, C., Glaser, P., Jacquet, C. & Martin, P., 2004, ‘Differentiation of the major Listeria monocytogenes Serovars by multiplex PCR differentiation of the major Listeria monocytogenes Serovars by multiplex PCR’, Journal of Clinical Microbiology 42(8), 3819–3822. https://doi.org/10.1128/JCM.42.8.3819-3822.2004
Doyle, M.P., Loneragan, G.H., Scott, H.M. & Singer, R.S., 2013, ‘Antimicrobial resistance: Challenges and perspectives’, Comprehensive Reviews in Food Science and Food Safety 12(2), 234–248. https://doi.org/10.1111/1541-4337.12008
Ducey, T.F., Page, B., Usgaard, T., Borucki, M.K., Pupedis, K. & Ward, T.J., 2006, ‘A single-nucleotide-polymorphism-based multilocus genotyping assay for subtyping lineage I Isolates of Listeria monocytogenes’, Applied and Environmental Microbiology 73(1), 133–147. https://doi.org/10.1128/AEM.01453-06
Duroux, A., Pimpie, R., Duez, J. & Milat, M., 2015, ‘Listeria phage and phage tail induction triggered by components of bacterial growth media (phosphate, LiCl, nalidixic acid, and acriflavine)’, Applied and Environmental Microbiology 81(6), 2117–2124. https://doi.org/10.1128/AEM.03235-14
El-Shenawy, M., El-Shenawy, M., Mañes, J. & Soriano, J.M., 2011, ‘Listeria spp. in street-vended ready-to-eat foods’, Interdisciplinary Perspectives on Infectious Diseases 2011(968031), 1–6. https://doi.org/10.1155/2011/968031
Ennaji, H., Timinouni, M., Ennaji, M.M., Hassar, M. & Cohen, N., 2008, ‘Characterization and antibiotic susceptibility of Listeria monocytogenes isolated from poultry and red meat in Morocco’, Infection and Drug Resistance 1, 45–50. https://doi.org/10.2147/idr.s3632
Eruteya, O.C. & Odunfa, S.A., 2014, ‘Original research article species and virulence determination of Listeria monocytogenes isolated from goat meat in Port Harcourt, Nigeria Listeria moncytogenes strains’, 3(5), 32–39.
Food and Authority, 2013, ‘Analysis of the baseline survey on the prevalence of Listeria monocytogenes in certain ready-to-eat foods in the EU, 2010–2011 Part A: Listeria monocytogenes prevalence estimates’, EFSA Journal 11(6), 3241. https://doi.org/10.2903/j.efsa.2013.3241
Food and Drug Administration, 2003, ‘Bacteriologycal analytical manual online. Detection and enumeration of Listeria monocytogenes in foods’, FDA, USA, Fecha de consulta: 27 de mayo de 2009.
Fouladynezhad, N., Afsah-Hejri, L., Rukayadi, Y., Abdulkarim, S.M., Marian, M.N. & Son, R., 2013, ‘Assessing biofilm formation by Listeria monocytogenes’, International Food Research Journal 20(2), 987–990.
Fox, E.M., Allnutt, T., Bradbury, M.I., Fanning, S. & Chandry, P.S., 2016, ‘Comparative genomics of the Listeria monocytogenes ST204 subgroup’, Frontiers in Microbiology 7, 2057. https://doi.org/10.3389/fmicb.2016.02057
Gasanov, U., Hughes, D. & Hansbro, P.M., 2005, ‘Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: A review’, FEMS Microbiology Reviews 29(5), 851–875. https://doi.org/10.1016/j.femsre.2004.12.002
Gill, D.A., 1937, ‘Ovine bacterial encephalitis (circling disease) and the bacterial genus Listerella’, Australian Veterinary Journal 13(2), 46–56. https://doi.org/10.1111/j.1751-0813.1937.tb01148.x
Gilmour, M.W., Graham, M., Domselaar, G., Van Tyler, S., Kent, H., Trout-yakel, K.M. et al., 2010, ‘High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak’. BMC Genomics 11(2010), 120. https://doi.org/10.1186/1471-2164-11-120
Gombas, D.E., Chen, Y., Clavero, R.S. & Scott, V.N., 2003, ‘Survey of Listeria monocytogenes in ready-to-eat foods’, Journal of Food Protection 66(4), 559–569. https://doi.org/10.4315/0362-028X-66.4.559
Gómez, D., Azón, E., Marco, N., Carramiñana, J.J., Rota, C., Ariño, A. et al., 2014, ‘Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment’, Food Microbiology 42(2014), 61–65. https://doi.org/10.1016/j.fm.2014.02.017
Gouin, E., Mengaud, J. & Cossart, P., 1994, ‘The virulence gene cluster of Listeria monocytogenes is also present in Listeria ivanovii, an animal pathogen, and Listeria seeligeri, a nonpathogenic species’, Infection and Immunity 62(8), 3550–3553. https://doi.org/10.1128/IAI.62.8.3550-3553.1994
Goulet, V., Hedberg, C., Le Monnier, A. & De Valk, H., 2008, ‘Increasing incidence of listeriosis in France and other European countries’, Emerging Infectious Diseases 14(5), 734–740. https://doi.org/10.3201/eid1405.071395
Grace, D., 2015, ‘Food safety in developing countries: An overview’, International Journal of Environmental Research and Public Health 12(9), 10490–10507. https://doi.org/10.3390/ijerph120910490
Gray, M.L. & Killinger, A.H., 1966, ‘Listeria monocytogenes and listeric infections’, Bacteriological Reviews 30(2), 309. https://doi.org/10.1128/MMBR.30.2.309-382.1966
Haase, J.K., Didelot, X., Lecuit, M., Korkeala, H., Achtman, M., Leclercq, A. et al., 2014, ‘The ubiquitous nature of Listeria monocytogenes clones: A large-scale Multilocus Sequence Typing study’, Environmental and Microbiology 16(2), 405–416. https://doi.org/10.1111/1462-2920.12342
Hain, T., Ghai, R., Billion, A., Kuenne, C.T., Steinweg, C., Izar, B. et al., 2012, Comparative genomics and transcriptomics of lineages I, II, and III strains of Listeria monocytogenes’, BMC Genomics 13, 144. https://doi.org/10.1186/1471-2164-13-144
Harakeh, S., Saleh, I., Zouhairi, O., Baydoun, E., Barbour, E. & Alwan, N., 2009, ‘Antimicrobial resistance of Listeria monocytogenes isolated from dairy-based food products’, Science of the Total Environment 407(13), 4022–4027. https://doi.org/10.1016/j.scitotenv.2009.04.010
Henri, C., Félix, B., Guillier, L., Leekitcharoenphon, P., Michelon, D., Mariet, J.-F. et al., 2016, ‘Population genetic structure of Listeria monocytogenes strains determined by pulsed-field gel electrophoresis and multilocus sequence typing’, Applied and Environmental Microbiology 82(18), 5720–5728. https://doi.org/10.1128/AEM.00583-16
Hernandez-Milian, A. & Payeras-Cifre, A., 2014, ‘What is new in listeriosis?’, BioMed Research International 2014(2014), 358051. https://doi.org/10.1155/2014/358051
Hilliard, A., Leong, D., Callaghan, A.O., Culligan, E.P., Morgan, C.A., Delappe, N. et al., 2018, ‘Genomic characterization of Listeria monocytogenes isolates associated with clinical listeriosis and the food production environment in Ireland’, Genes 9(3), 171. https://doi.org/10.3390/genes9030171
Holch, A., Webb, K., Lukjancenko, O., Ussery, D. & Rosenthal, B.M., 2013, ‘Genome sequencing identifies two nearly unchanged strains of persistent Listeria monocytogenes isolated at two different fish processing plants sampled 6 years apart’, Applied and Environmental Microbiology 79(9), 2944–2951. https://doi.org/10.1128/AEM.03715-12
Hopkins, K.L., Arnold, C. & Threlfall, E.J., 2007, ‘Rapid detection of gyrA and parC mutations in quinolone-resistant Salmonella enterica using Pyrosequencing® technology’, Journal of Microbiological Methods 68(1), 163–171. https://doi.org/10.1016/j.mimet.2006.07.006
Hülphers, G., 1911, ‘Liver necrosis in rabbits caused by a hitherto undescribed bacterium’, Swedish Veterinary Journal 16(1911), 265–273.
Indrawattana, N., Nibaddhasobon, T., Sookrung, N., Chongsa-nguan, M., Tungtrongchitr, A., Makino, S., et al., 2011, ‘Prevalence of Listeria monocytogenes in raw meats marketed in Bangkok and characterization of the isolates by phenotypic and molecular methods’, Journal of Health, Population and Nutrition 29(1), 26–38. https://doi.org/10.3329/jhpn.v29i1.7565
Ismaiel, A.A.R., Ali, A.E.S. & Enan, G., 2014, ‘Incidence of Listeria in Egyptian meat and dairy samples’, Food Science and Biotechnology 23(1), 179–185. https://doi.org/10.1007/s10068-014-0024-5
ISO, International Standards Organisation 11290–1:2014, Microbiology of food and animal feeding stuffs-horizontal method for the detection and enumeration of Listeria monocytogenes – Part 1: Detection Method, South African Bureau of Standards, Pretoria.
Jadhav, S., 2015, ‘Detection, subtyping and control of Listeria monocytogenes in food processing environments’, Doctoral dissertation, Melbourne, Swinburne University of Technology.
Jemal, T.H., 2014, ‘Prevalence and antibiotic susceptibility of Listeria species in raw milk and dairy products from north shewa zone, oromia regional state’, Master dissertation, Oromia Regional State Haramaya University.
Jersek, B., Gilot, P., Gubina, M., Klun, N., Mehle, J., Rijpens, N. et al., 1999, ‘Typing of Listeria monocytogenes strains by repetitive element sequence-based PCR typing of Listeria monocytogenes strains by repetitive element sequence-based PCR’, Journal of Clinical Microbiology 37(1), 103–109. https://doi.org/10.1128/JCM.37.1.103-109.1999
Jeyaletchumi, P., Tunung, R., Selina, P.M., Chai, L.C., Radu, S., Farinazleen, M.G. et al., 2012, ‘Assessment of Listeria monocytogenes in salad vegetables through kitchen simulation study’, International Food Reseach Journal 17(1), 1–11.
Jooste, P., Jordan, K., Leong, D. and Alvarez-Ordóñez, A., 2016, ‘Listeria monocytogenes in food: Control by monitoring the food processing environment’, African Journal of Microbiology Research 10(1), 1–14.
Kalpana, K. & Muriana, P.M., 2002, Subtyping of Listeria monocytogenes by multilocus sequence typing and pulsed-field gel electrophoresis (PFGE), Aminal Science Report, Oklahama State University Publication (1008), Stillwater, Oklahoma.
Klumpp, J. & Loessner, M.J., 2013, ‘Genomes, evolution, and application Listeria phages’, Bacteriophage 3(3), e26861. https://doi.org/10.4161/bact.26861
Korthals, M., Ege, M., Lick, S., Von Mutius, E. & Bauer, J., 2008, ‘Occurrence of Listeria spp. in mattress dust of farm children in Bavaria’, Environmental Research 107(3), 299–304. https://doi.org/10.1016/j.envres.2008.02.007
Kovacevic, J., Sagert, J., Wozniak, A., Gilmour, M.W. & Allen, K.J., 2013, ‘Antimicrobial resistance and co-selection phenomenon in Listeria spp. recovered from food and food production environments’, Food Microbiology 34(2), 319–327. https://doi.org/10.1016/j.fm.2013.01.002
Kramarenko, T., Roasto, M., Meremäe, K., Kuningas, M., Põltsama, P. & Elias, T., 2013, ‘Listeria monocytogenes prevalence and serotype diversity in various foods’, Food Control 30(1), 24–29. https://doi.org/10.1016/j.foodcont.2012.06.047
Kyoui, D., Takahashi, H., Miya, S., Kuda, T. & Kimura, B., 2014, ‘Comparison of the major virulence-related genes of Listeria monocytogenes in Internalin A truncated strain 36-25-1 and a clinical wild-type strain’, BMC Microbiology 14(15), 1417–2180. https://doi.org/10.1186/1471-2180-14-15
Lacroix, C., Meile, L., Bertsch, D., Muelli, M. & Weller, M., 2014, ‘Antimicrobial susceptibility and antibiotic resistance gene transfer analysis of foodborne, clinical, and environmental Listeria spp. isolates including Listeria monocytogenes’, FEMS Microbiology Ecoloy 78(2), 210–219.
Laksanalamai, P., Huang, B., Sabo, J., Burall, L.S., Zhao, S., Bates, J. et al., 2014, ‘Genomic characterization of novel Listeria monocytogenes serotype 4b variant strains’, PLoS One 9(2), e89024. https://doi.org/10.1371/journal.pone.0089024
Lambertz, S.T., Nilsson, C., Brådenmark, A., Sylvén, S., Johansson, A., Jansson, L.M. et al., 2012, ‘Prevalence and level of Listeria monocytogenes in ready-to-eat foods in Sweden 2010’, International Journal of Food Microbiology 160(1), 24–31.
Lamont, R. & Sobel, J., 2011, ‘Listeriosis in human pregnancy: A systematic review’, Journal of Perinatal Medicine 39(3), 227–236.
Lekkas, P., 2016, ‘The Microbial Ecology Of Listeria monocytogenes As impacted by three environments: A cheese microbial community; a farm environment; and a soil microbial community’, Doctoral dissertation, Burlington, University of Vermont, Vermont.
Leong, D., Alvarez-Ordóñez, A. & Jordan, K., 2014, ‘Monitoring occurrence and persistence of Listeria monocytogenes in foods and food processing environments in the Republic of Ireland’, Frontiers in Microbiology 5(436), 1–8. https://doi.org/10.3389/fmicb.2014.00436
Leong, D., NicAogáin, K., Luque-Sastre, L., McManamon, O., Hunt, K., Alvarez-Ordóñez, A. et al., 2017, ‘A 3-year multi-food study of the presence and persistence of Listeria monocytogenes in 54 small food businesses in Ireland’, International Journal of Food Microbiology 249, 18–26. https://doi.org/10.1016/j.ijfoodmicro.2017.02.015
Li, Z., Pérez-Osorio, A., Wang, Y., Eckmann, K., Glover, W.A., Allard, M.W. et al., 2017, ‘Whole genome sequencing analyses of Listeria monocytogenes that persisted in a milkshake machine for a year and caused illnesses in Washington State’, BMC Microbiology 17(1), 134. https://doi.org/10.1186/s12866-017-1043-1
Lindstedt, B.A., Tham, W., Danielsson-Tham, M.L., Vardund, T., Helmersson, S. & Kapperud, G., 2008, ‘Multiple-locus variable-number tandem-repeats analysis of Listeria monocytogenes using multicolour capillary electrophoresis and comparison with pulsed-field gel electrophoresis typing’, Journal of Microbiological Methods 72(2), 141–148. https://doi.org/10.1016/j.mimet.2007.11.012
Linke, K., Rückerl, I., Brugger, K., Karpiskova, R., Walland, J., Muri-Klinger, S. et al., 2014, ‘Reservoirs of Listeria species in three environmental ecosystems’, Applied and Environment Microbiology 80(18), 5583–5592. https://doi.org/10.1128/AEM.01018-14
Liu, D., 2006, ‘Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen’, Journal of Medical Microbiology 55(6), 645–659. https://doi.org/10.1099/jmm.0.46495-0
Liu, D., Lawrence, M.L., Austin, F.W. & Ainsworth, A.J., 2007, ‘A multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes’, Journal of Microbiological Methods 71(2), 133–140. https://doi.org/10.1016/j.mimet.2007.08.007
Loman, N.J. (2012), ‘Comparative bacterial genomics’, Doctoral desertation, Birmingham, University of Birmingham, United Kingdom.
Lourenço, A., Neves, E. & Brito, L., 2009, ‘Susceptibility of Listeria monocytogenes from traditional cheese-dairies to in-use sanitizers’, Food Control 20(6), 585–589. https://doi.org/10.1016/j.foodcont.2008.08.009
Maertens de Noordhout, C., Devleesschauwer, B., Angulo, F.J., Verbeke, G., Haagsma, J., Kirk, M. et al., 2014, ‘The global burden of listeriosis: A systematic review and meta-analysis’, Lancet Infectious Diseases14(11), 1073–1082.gcina https://doi.org/10.1016/S1473-3099(14)70870-9
Magwedere, K., Songabe, T. & Dziva, F., 2015, ‘Challenges of sanitary compliance related to trade in products of animal origin in Southern Africa’, Italian Journal of Food Safety 4(3), 107–114. https://doi.org/10.4081/ijfs.2015.5114
Mammina, C., Parisi, A., Guaita, A., Aleo, A., Bonura, C., Nastasi, A. et al., 2013, ‘Enhanced surveillance of invasive listeriosis in the Lombardy region, Italy, in the years 2006–2010 reveals major clones and an increase in serotype ½a’, BMC Infectious Diseases 13, 152(2013). https://doi.org/10.1186/1471-2334-13-152
Martín, B., Perich, A., Gómez, D., Yangüela, J., Rodríguez, A., Garriga, M. 2014, ‘Diversity and distribution of Listeria monocytogenes in meat processing plants’, Food Microbiology 44(2014), 119–127. https://doi.org/10.1016/j.fm.2014.05.014
Mata, M.T., Baquero, F. & Pe, J.C., 2000, ‘A multidrug transporter in Listeria monocytogenes’, FEMS, Microbiology, Letters 187(2), 185–188. https://doi.org/10.1111/j.1574-6968.2000.tb09158.x
Mateus, T., Silva, J., Maia, R.L. & Teixeira, P., 2013, ‘Listeriosis during pregnancy: A public health concern’, ISRN Obstetrics and Gynecology 2013(2013), 851712, 1–6. https://doi.org/10.1155/2013/851712
Matle, I., 2016, ‘The relationship between hygiene assessment system audit scores and the bacteriological status of single species red meat abattoirs in the Free State province’, Master dissertation, Central University of Technology, Free State, Bloemfontein.
Matle, I., Mbatha, K.R., Lentsoane, O., Magwedere, K., Morey, L. & Madoroba, E., 2019, ‘Occurrence, serotypes, and characteristics of Listeria monocytogenes in meat and meat products in South Africa between 2014 and 2016’, Journal of Food Safety 39(4), e12629. https://doi.org/10.1111/jfs.12629
Mitchell, J.A., Pirie, J.H. & Ingram, A., 1927, ‘The plague problem in South Africa: Historical, bacteriological and entomological studies’, Publications of the South African Institute for Medical Research 3(20), 309–384.
Miya, S., Takahashi, H., Nakagawa, M., Kuda, T. & Igimi, S., 2015, ‘Genetic characteristics of Japanese clinical Listeria monocytogenes isolates’, PLoS One 10(3), e0122902. https://doi.org/10.1371/journal.pone.0122902
Mizuno, S., Zendejas, I.R., Reed, A.I., Kim, R.D., Howard, R.J., Hemming, A.W. et al., 2007, ‘Listeria monocytogenes following orthotopic liver transplantation: Central nervous system involvement and review of the literature’, World Journal of Gastroenterology: WJG 13(32), 4391. https://doi.org/10.3748/wjg.v13.i32.4391
Moreno, L.Z., Paixão, R., Gobbi, D.D.S., Raimundo, D.C., Ferreira, T.P., Moreno, A.M. et al. 2014 ‘Characterization of antibiotic resistance in Listeria spp. isolated from slaughterhouse environments, pork and human infections’, Journal of Infection in Developing Countries8(4), 416–423. https://doi.org/10.3855/jidc.4188
Møretrø, T., Langsrud, S. & Heir, E., 2013, ‘Bacteria on meat abattoir process surfaces after sanitation: Characterisation of survival properties of Listeria monocytogenes and the commensal bacterial flora’, Advances in Microbiology 3(03), 255. https://doi.org/10.4236/aim.2013.33037
Morobe, I.C., Obi, C.L., Nyila, M., Matsheka, M.I. & Gashe, B., 2006, ‘Molecular characterization and serotyping of Listeria monocytogenes with a focus on food safety and disease prevention’, Biochemical Testing 8(2006), 197–216.
Morobe, I.C., Obi, C.L., Nyila, M.A., Gashe, B.A. & Matsheka, M.I., 2009, ‘Prevalence, antimicrobial resistance profiles of Listeria monocytognes from various foods in Gaborone, Botswana’, African Journal of Biotechnology 8(22), 285. https://doi.org/10.5897/AJB2009.000-9486
Murphy, M., Corcoran, D., Buckley, J.F., O’Mahony, M., Whyte, P. & Fanning, S., 2007, ‘Development and application of multiple-locus variable number of tandem repeat analysis (MLVA) to subtype a collection of Listeria monocytogenes’, International Journal of Food Microbiology 115(2), 187–194. https://doi.org/10.1016/j.ijfoodmicro.2006.10.022
Murray, E.G.D., Webb, R.A. & Swann, M.B.R., 1926, ‘A disease of rabbits characterised by a large mononuclear leucocytosis, caused by a hitherto undescribed bacillus Bacterium monocytogenes (n. sp.)’, The Journal of Pathology and Bacteriology 29(4), 407–439. https://doi.org/10.1002/path.1700290409
Nappi, R., Bozzetta, E., Serra, R., Grattarola, C., Decastelli, L., Florio, C. et al., 2005, ‘Molecular characterization of listeria monocytogenes strains associated with outbreaks of listeriosis in humans and ruminants and food products by serotyping and automated ribotyping’, Veterinary Research Communications 29(Suppl 2), 249–252. https://doi.org/10.1007/s11259-005-0054-9
Nel, H., Van Vuuren, M. & Swan, G., 2004, ‘Towards the establishment and standardization of a veterinary antimicrobial resistance surveillance and monitoring programme in South Africa’, Onderstepoort Journal of Veterinary Research 71(3), 239–246. https://doi.org/10.4102/ojvr.v71i3.266
Neves, D., Job, V., Dortet, L., Cossart, P. & Dessen, A., 2013, ‘Structure of internalin InlK from the human pathogen Listeria monocytogenes’, Journal of Molecular Biology 425(22), 4520–4529. https://doi.org/10.1016/j.jmb.2013.08.010
Nho, S.W., Abdelhamed, H., Reddy, S., Karsi, A. & Lawrence, M.L., 2015, ‘Identification of high-risk Listeria monocytogenes serotypes in lineage I (serotype ½a, ½c, 3a and 3c) using multiplex PCR’, Journal of Applied Microbiology 119(3), 845–852. https://doi.org/10.1111/jam.12876
Nightingale, K.K., Schukken, Y.H., Nightingale, C.R., Fortes, E.D., Ho, A.J., Her, Z., Grohn, Y.T., McDonough, P.L. & Wiedmann, M., 2004, ‘Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment’, Applied Environmental Microbiology 70(8), 4458–4467. https://doi.org/10.1128/AEM.70.8.4458-4467.2004
Noll, M., Kleta, S. & Al, S., 2018, ‘Antibiotic susceptibility of Listeria monocytogenes strains isolated from food, food-processing plants and human samples in Germany’, Journal of Infection and Public Health 11(4), 572–577. https://doi.org/10.1016/j.jiph.2017.12.007
Nørrung, B. & Buncic, S., 2008, ‘Microbial safety of meat in the European Union’, Meat Science 78(1–2), 14–24. https://doi.org/10.1016/j.meatsci.2007.07.032
Ntivuguruzwa, J.B., 2016, ‘Molecular characterization and antimicrobial resistance profiles of Salmonella Typhimurium isolated between 1995 and 2002 from organs and environments of diseased poultry in South Africa’, Master dissertation, University of Pretoria, Pretoria.
Nyarko, E.B. & Donnelly, C.W., 2015, ‘JFS special issue: 75 years of advancing food science, and preparing for the next 75: Listeria monocytogenes: Strain heterogeneity, methods, and challenges of subtyping’, Journal of Food Science 80(12), M2868–M2878. https://doi.org/10.1111/1750-3841.13133
Nyfeldt, A., 1929, ‘Etiologie de la mononucleose infectieuse’, PubMed Journal 101(1929), 590–591.
O’Connor, L., O’Leary, M., Leonard, N., Godinho, M., O’Reilly, C., Egan, J. et al., 2010, ‘The characterization of Listeria spp. isolated from food products and the food-processing environment’, Letters in Applied Microbiology 51(5), 490–498. https://doi.org/10.1111/j.1472-765X.2010.02928.x
Obaidat, M.M., Salman, A.E.B. & Lafi, S.Q., 2015, ‘Characterization of Listeria monocytogenes from three countries and antibiotic resistance differences among countries and Listeria monocytogenes serogroups’, Letters in Applied Microbiology 60(6), 609–614. https://doi.org/10.1111/lam.12420
Okutani, A., Okada, Y., Yamamoto, S. & Igimi, S., 2004, ‘Nationwide survey of human Listeria monocytogenes infection in Japan’, Epidemiology and Infection 132(4), 769–772. https://doi.org/10.1017/S0950268804001967
Orsi, R.H., Bakker, H.C & Wiedmann, M., 2011, ‘Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics’, International Journal of Medical Microbiology 301(2), 79–96. https://doi.org/10.1016/j.ijmm.2010.05.002
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(2008), 1–17. https://doi.org/10.1186/1471-2164-9-539
Pan, Y., Breidt, F. and Kathariou, S., 2006, ‘Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment’, Applied and Environmental Microbiology 72(12), 7711–7717.
Parihar, V.S., 2004, ‘Zoonotic aspects of Listeria monocytogenes with special reference to bacteriology’, Master dissertation, Swedish University of Agricultural Sciences.
Pava-Ripoll, M., Pearson, R.E.G., Miller, A.K. & Ziobro, G.C., 2012, ‘Prevalence and relative risk of Cronobacter spp., Salmonella spp., and Listeria monocytogenes associated with the body surfaces and guts of individual filth flies’, Applied and Environmental Microbiology 78(22), 7891–7902. https://doi.org/10.1128/AEM.02195-12
Piet, J., Kieran, J., Dara, L. & Avelino, A.O, 2016, ‘Listeria monocytogenes in food: Control by monitoring the food processing environment’, African Journal of Microbiology Research 10(1), 1–14. https://doi.org/10.5897/AJMR2015.7832
Poimenidou, S.V., Dalmasso, M., Papadimitriou, K., Fox, E.M., Skandamis, P. & Jordan, K., 2018, ‘Virulence gene sequencing highlights similarities and differences in sequences in Listeria monocytogenes serotype ½a and 4b strains of clinical and food origin from 3 different geographic locations’, Frontiers in Microbiology 9, 1103(2018). https://doi.org/10.3389/fmicb.2018.01103
Popovic, I., Heron, B. & Covacin, C., 2014, ‘Listeria: an Australian perspective (2001–2010)’, Foodborne Pathogens and Disease 11(6), 425–432. https://doi.org/10.1089/fpd.2013.1697
Pournajaf, A., Rajabnia, R., Sedighi, M., Kassani, A., Moqarabzadeh, V., Lotfollahi, L. et al., 2016, ‘Prevalence, and virulence determination of Listeria monocytogenes strains isolated from clinical and non-clinical samples by multiplex polymerase chain reaction’, Revista da Sociedade Brasileira de Medicina Tropical 49(5), 624–627. https://doi.org/10.1590/0037-8682-0403-2015
Pushkareva, V.I. & Ermolaeva, S.A., 2010, ‘Listeria monocytogenes virulence factor Listeriolysin O favors bacterial growth in co-culture with the ciliate Tetrahymena pyriformis, causes protozoan encystment and promotes bacterial survival inside cysts’, BMC Microbiology 10, 26(2010). https://doi.org/10.1186/1471-2180-10-26.
Quendera, A.P., Varela, C., Barreto, A.S. & Semedo-Lemsaddek, T., 2016, ‘Characterization of Listeria monocytogenes from food and food-related settings’, International Food Research Journal 23(2), 909–912.
Rabinovich, L., Sigal, N., Borovok, I., Nir-Paz, R. & Herskovits, A.A., 2012, ‘Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence’, Cell 150(4), 792–802. https://doi.org/10.1016/j.cell.2012.06.036
Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Monnier, A. et al., 2008, ‘A new perspective on Listeria monocytogenes evolution’, PLoS Pathogens 4(9), e100014. https://doi.org/10.1371/journal.ppat.1000146
Rahimi, E., Momtaz, H., Sharifzadeh, A., Behzadnia, A., Ashtari, M.S., Esfahani, S.Z. et al., 2012, ‘Prevalence and antimicrobial resistance of Listeria species isolated from traditional dairy products in chahar mahal & bakhtiyari, Iran’, Food Control 21(11), 1448–1452. https://doi.org/10.1016/j.foodcont.2010.03.014
Rantsiou, K., Alessandria, V., Urso, R., Dolci, P. & Cocolin, L., 2008, ‘Detection, quantification and vitality of Listeria monocytogenes in food as determined by quantitative PCR’, International Journal of Food Microbiology 121(1), 99–105. https://doi.org/10.1016/j.ijfoodmicro.2007.11.006
Revazishvili, T., Kotetishvili, M., Stine, O.C., Kreger, A.S., Jr, J.G.M., Morris, J.G. et al., 2004, ‘Comparative analysis of multilocus sequence typing and pulsed-field gel electrophoresis for characterizing Listeria monocytogenes strains isolated from environmental and clinical sources’, Journal of Clinical Microbiology 42(1), 276–285. https://doi.org/10.1128/JCM.42.1.276-285.2004
Rip, D., 2011, ‘The implementation of sub-typing techniques to determine the diversity of L. monocytogenes strains adapted to the food processing environment and their association with human listeriosis cases’, Doctoral dissertation, University of the Western Cape, Cape Town.
Roberts, A., Nightingale, K., Jeffers, G., Fortes, E., Kongo, J.M., Wiedmann, M. et al., 2018, ‘Genetic and phenotypic characterization of Listeria monocytogenes lineage III’, Microbiology 152(3), 685–693. https://doi.org/10.1099/mic.0.28503-0
Ruppitsch, W., Pietzka, A., Prior, K., Bletz, S., Fernandez, H.L., Allerberger, F. et al., 2015, ‘Defining and evaluating a core genome multilocus sequence typing scheme for whole-genome sequence-based typing of Listeria monocytogenes’, Journal of Clinical Microbiology 53(9), 2869–2876.
Ryan, S., Begley, M., Hill, C. & Gahan, C.G.M., 2010, ‘A five-gene stress survival islet (SSI-1) that contributes to the growth of Listeria monocytogenes in suboptimal conditions’, Journal of Applied Microbiology 109(3), 984–995. https://doi.org/10.1111/j.1365-2672.2010.04726.x
Ryu, J., Park, S.H., Yeom, Y.S., Shrivastav, A., Lee, S.H., Kim, Y.R. et al., 2013, ‘Simultaneous detection of Listeria species isolated from meat processed foods using multiplex PCR’, Food Control 32(2), 659–664. https://doi.org/10.1016/j.foodcont.2013.01.048
Sabet, C., Lecuit, M., Cabanes, D., Cossart, P. & Bierne, H., 2005, ‘LPXTG protein InlJ, a newly identified internalin involved in Listeria monocytogenes virulence’, Infection and Immunity 73(10), 6912–6922. https://doi.org/10.1128/IAI.73.10.6912-6922.2005
Salcedo, C., Arreaza, L., Alcala, B., De Fuente, L. & Va, J.A., 2003, ‘Development of a multilocus sequence typing method for analysis of Listeria monocytogenes clones’, 41(2), 757–762. https://doi.org/10.1128/JCM.41.2.757-762.2003
Sauders, B.D., Overdevest, J., Fortes, E., Windham, K., Schukken, Y., Lembo, A. et al., 2012, ‘Diversity of Listeria species in urban and natural environments’, Applied and Environment Microbiology 78(12), 4420–4433. https://doi.org/10.1128/AEM.00282-12
Sauders, B.D., Sanchez, M.D., Rice, D.H., Corby, J., Stich, S., Fortes, E.D. et al., 2016, ‘Prevalence and molecular diversity of Listeria monocytogenes in Retail Establishments’, Journal of Food Protection 72(11), 2337–2349. https://doi.org/10.4315/0362-028X-72.11.2337
Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R. V., Widdowson, M.A., Roy, S.L. et al, 2011, ‘Foodborne illness acquired in the United States-Major pathogens’, Emerging Infectious Diseases 17(1), 7–15. https://doi.org/10.3201/eid1701.P11101
Schmid, D., Allerberger, F., Huhulescu, S., Pietzka, A., Amar, C., Kleta, S. et al., 2014, ‘Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011–2013’, Clinical Microbiology and Infection 20(5), 431–436. https://doi.org/10.1111/1469-0691.12638
Schmitz-Esser, S., Miller, A., Stessl, B. & Wagner, M., 2015, ‘Genomes of sequence type 121 Listeria monocytogenes strains harbor highly conserved plasmids and prophages’, Frontiers in Microbiology 6(380). https://doi.org/10.3389/fmicb.2015.00380.
Schwartz, B., Hexter, D., Broome, C.V, Hightower, A.W., Hirschhorn, R.B., Porter, J.D. et al., 2018, Investigation of an outbreak of listeriosis: New Hypotheses for the etiology of epidemic Listeria monocytogenes Infections and David G, Oxford University Press, Faris, viewed from http://www.jstor.org/stable/30137096 Investigation of an Ou.
Scortti, M., Han, L., Alvarez, S., Leclercq, A., Moura, A., Lecuit, M. et al., 2018, ‘Epistatic control of intrinsic resistance by virulence genes in Listeria’, PLoS Genetics 14(9), e1007525. https://doi.org/10.1371/journal.pgen.1007525
Shaker, E.M. & Hassanien, A.A., 2015, ‘PCR Techniques detection of some virulence associated genes in Listeria monocytogenes isolated from table eggs and clinical human samples’, Assiut Veterinary Medical Journal 61(2015), 219–225.
Silk, B.J., Mahon, B.E., Griffin, P.M., Gould, L.H., Tauxe, R.V., Crim, S.M. et al., 2013, ‘Vital signs: Listeria illnesses, deaths, and outbreaks – United States, 2009–2011’, MMWR. Morbidity and Mortality Weekly Report 62(22), 448. https://doi.org/10.1016/j.annemergmed.2013.08.006
Siu, L.K., Lu, P.L., Chen, J.Y., Lin, F.M. & Chang, S.C., 2003, ‘High-level expression of AmpC β-lactamase due to insertion of nucleotides between -10 and -35 promoter sequences in Escherichia coli clinical isolates: Cases not responsive to extended-spectrum-cephalosporin treatment’, Antimicrobial Agents and Chemotherapy 47(7), 2138–2144. https://doi.org/10.1128/AAC.47.7.2138-2144.2003
Smith, A.M., Tau, N.P., Smouse, S.L., Allam, M., Ismail, A., Ramalwa, N.R. et al., 2019, ‘Outbreak of Listeria monocytogenes in South Africa, 2017–2018: Laboratory Activities and Experiences Associated with Whole-Genome Sequencing Analysis of Isolates’, Foodborne Pathogens and Disease 16(7), 524–530. http://doi.org/10.1089/fpd.2018.2586
Sofos, J.N. & Geornaras, I., 2010, ‘Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Escherichia coli O157:H7 in nonintact, and Listeria monocytogenes in ready-to-eat, meat products’, Meat Science 86(1), 2–14. https://doi.org/10.1016/j.meatsci.2010.04.015
Soni, D.K., Singh, M., Singh, D.V. & Dubey, S.K., 2014, ‘Virulence and genotypic characterization of Listeria monocytogenes isolated from vegetable and soil samples’, BMC Microbiology 14(1), 241. https://doi.org/10.1186/s12866-014-0241-3
Strydom, A., 2015, ‘Control of Listeria monocytogenes in an avocado processing facility’, Doctoral dissertation, University of the Free State, Bleomfontein.
Susana, C., Cláudia, R., Gonçalves, V. & De Sá, C., 2017, ‘An overview of Listeria monocytogenes contamination in ready to eat meat, dairy and fishery foods’, Ciência Rural 47(2), 1–8. https://doi.org/10.1590/0103-8478cr20160721
Takahashi, H., Ohshima, C., Nakagawa, M., Thanatsang, K., Phraephaisarn, C., Chaturongkasumrit, Y. et al., 2014, ‘Development of new multilocus variable number of tandem repeat analysis (MLVA) for Listeria innocua and its application in a food processing plant’, PLoS One 9(9), 1–7. https://doi.org/10.1371/journal.pone.0105803
Thévenot, D., Dernburg, A. & Vernozy-Rozand, C., 2006, ‘An updated review of Listeria monocytogenes in the pork meat industry and its products’, Journal of Applied Microbiology 101(1), 7–17. https://doi.org/10.1111/j.1365-2672.2006.02962.x
Todd, E.C.D. & Notermans, S., 2011, ‘Surveillance of listeriosis and its causative pathogen, Listeria monocytogenes’, Food Control 22(9), 1484–1490. https://doi.org/10.1016/j.foodcont.2010.07.021
Truter, I., 2015, ‘Antimicrobial prescribing in South Africa using a large pharmacy database: A drug utilisation study Ilse Truter’, Southern African Journal of Infectious Diseases 30(2), 52–56. https://doi.org/10.1080/23120053.2015.1054181
Välimaa, A.L., Tilsala-Timisjärvi, A. & Virtanen, E., 2015, ‘Rapid detection and identification methods for Listeria monocytogenes in the food chain–A review’, Food Control 55(2015), 103–114. https://doi.org/10.1016/j.foodcont.2015.02.037
Van Vuuren, M., 2001, ‘Antibiotic resistance, with special reference to poultry production’, OIE 2001, 135–146.
Vasconcelos, R.M.D., Almeida, A.E.C.C.D., Hofer, E., Silva, N.M.M.D. & Marin, V.A., 2008, ‘Multiplex-PCR serotyping of Listeria monocytogenes isolated from human clinical specimens’, Memórias do Instituto Oswaldo Cruz 103(8), 836–838. https://doi.org/10.1590/S0074-02762008000800016
Vázquez-Boland, J., Kuhn, M., Berche, P., Chakraborty, T., Domi, G., González-zorn, B. et al., 2001, ‘Listeria pathogenesis and molecular virulence determinants Listeria pathogenesis and molecular virulence determinants’, Clinical Microbiology. Reviews 14(3), 584–640. https://doi.org/10.1128/CMR.14.3.584-640.2001
Verraes, C., Van Boxstael, S., Van Meervenne, E., Van Coillie, E., Butaye, P., Catry, B. et al., 2013, ‘Antimicrobial resistance in the food chain: A review’, International Journal of Environmental Research and Public Health 10(7), 2643–2669. https://doi.org/10.3390/ijerph10072643
Vitas, A.I. & Garcia-jalon, V.A.I., 2004, ‘Occurrence of Listeria monocytogenes in fresh and processed foods in Navarra (Spain)’, International Journal of Food Microbiology 90(3), 349–356. https://doi.org/10.1016/S0168-1605(03)00314-3
Volpe Sperry, K.E., Kathariou, S., Edwards, J.S. & Wolf, L.A., 2008, ‘Multiple-locus variable-number tandem-repeat analysis as a tool for subtyping Listeria monocytogenes strains’, Journal of Clinical Microbiology 46(4), 1435–1450. https://doi.org/10.1128/JCM.02207-07
Walsh, D., Duffy, G., Sheridan, J.J., Blair, I.S. & McDowell, D.A., 2001, ‘Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail food’, Journal of Applied Microbiology 90(4), 517–522. https://doi.org/10.1046/j.1365-2672.2001.01273.x
Wang, Y., Zhao, A., Zhu, R., Lan, R., Jin, D., Cui, Z. et al., 2012, ‘Genetic diversity and molecular typing of Listeria monocytogenes in China’, BMC Microbiology 12(1), 119. https://doi.org/10.1186/1471-2180-12-119
Werbrouck, H., Grijspeerdt, K., Botteldoorn, N., Van Pamel, E., Rijpens, N., Van Damme, J. et al., 2006, ‘Differential inlA and inlB expression and interaction with human intestinal and liver cells by Listeria monocytogenes strains of different origins’, Applied and Environmental Microbiology 72(6), 3862–3871. https://doi.org/10.1128/AEM.02164-05
WHO, World Organization for Animal Health, 2014, Listeria monocytogenes, OIE Terrestrial Manual 2014, Chapter 2, pp. 1–18, viewed 14 September 2020, https://www.oie.int/standard-setting/terrestrial-manual/access-online/.
Wieczorek, K., Dmowska, K. & Osek, J., 2012, ‘Prevalence, characterization, and antimicrobial resistance of Listeria monocytogenes isolates from bovine hides and carcasses’, Applied and Environmental Microbiology 78(6), 2043–2045. https://doi.org/10.1128/AEM.07156-11
Willaarts, B., Pardo, I. & De la Mora, G., 2013, ‘Urbanization, socio-economic changes and population growth in Brazil: dietary shifts and environmental implications’, XXVII IUSSP International Population Conference, pp. 1–18. Busan.
Wilson, A., Gray, J., Chandry, P.S. & Fox, E.M., 2018, ‘Phenotypic and genotypic Analysis of antimicrobial resistance among Listeria monocytogenes isolated from Australian food production chains’, Genes 9(2), 80. https://doi.org/10.3390/genes9020080.
Yu, T., Jiang, X., Zhang, Y., Ji, S., Gao, W. & Shi, L., 2018, ‘Effect of benzalkonium chloride adaptation on sensitivity to antimicrobial agents and tolerance to environmental stresses in Listeria monocytogenes’, Frontiers in Microbiology 9(2018), 2906.
Zhang, W., Jayarao, B.M. & Knabel, S.J., 2004, ‘Multi-virulence-locus sequence typing of Listeria monocytogenes’, Applied and Environmental Microbiology 70(2), 913–920. https://doi.org/10.1128/AEM.70.2.913-920.2004
Zhu, Q., Gooneratne, R. & Hussain, M., 2017, ‘Listeria monocytogenes in fresh produce: Outbreaks, prevalence and contamination levels’, Foods 6(3), 21. https://doi.org/10.3390/foods6030021
Zuber, I., Lakicevic, B., Pietzka, A., Milanov, D. & Djordjevic, V., 2019, ‘Molecular characterization of Listeria monocytogenes isolates from a small- scale meat processor in Montenegro, 2011–2014’, Journal Of Food Microbiology 79(2019), 116–122. https://doi.org/10.1016/j.fm.2018.12.005
|
Email this article 
Hide
Show all
