Implicated Food Products for Listeriosis and Changes in Serovars of Listeria monocytogenes Affecting Humans in Recent Decades

Abstract

Listeriosis is a foodborne disease with a high fatality rate, and infection is mostly transmitted through ready-to-eat (RTE) foods contaminated with Listeria monocytogenes, such as gravad/smoked fish, soft cheeses, and sliced processed delicatessen (deli) meat. Food products/dishes stored in vacuum or in modified atmospheres and with extended refrigerator shelf lives provide an opportunity for L. monocytogenes to multiply to large numbers toward the end of the shelf life. Elderly, pregnant women, neonates, and immunocompromised individuals are particularly susceptible to L. monocytogenes. Listeriosis in humans manifests primarily as septicemia, meningitis, encephalitis, gastrointestinal infection, and abortion. In the mid 1990s and early 2000s a shift from L. monocytogenes serovar 4b to serovar 1/2a causing human listeriosis occurred, and serovar 1/2a is becoming more frequently linked to outbreaks of listeriosis, particularly in Europe and Northern America. Consumer lifestyle has changed, and less time is available for food preparation. Modern lifestyle has markedly changed eating habits worldwide, with a consequent increased demand for RTE foods; therefore, more RTE and take away foods are consumed. There is a concern that many Listeria outbreaks are reported from hospitals. Therefore, it is vitally important that foods (especially cooked and chilled) delivered to hospitals and residential homes for senior citizens and elderly people are reheated to at least 72°C: cold food, such as turkey deli meat and cold-smoked and gravad salmon should be free from L. monocytogenes. Several countries have zero tolerance for RTE foods that support the growth of Listeria.

Listeriosis Today

Listeriosis is a foodborne disease that is mostly transmitted through ready-to-eat (RTE) foods contaminated with Listeria monocytogenes (and more rarely with other Listeria species) such as gravad/smoked fish, soft cheeses, and delicatessen (deli) meats (Lopez-Valladares et al., 2014; Raheem, 2016). The new generations of refrigerated RTE foods posing concern for listeriosis are products with no inhibitory organic acids or those lacking high counts of competing microorganisms and with an extended shelf life. RTE foods are normally eaten without further bactericidal treatment (Luber et al., 2011). L. monocytogenes is psychrotrophic and can grow without oxygen; therefore, food products/dishes stored in vacuum or in modified atmospheres with extended refrigerator shelf life provide an opportunity for L. monocytogenes to multiply to large numbers toward the end of the shelf life, without having to compete with other foodborne microorganisms (Lado and Yousef, 2007; Baka et al., 2015).

Listeriosis affected about 2200 people in 2015, causing 270 deaths (12.3%)—the highest number ever reported in the EU (EFSA, 2016). Fatality is highest in susceptible populations with underlying immunosuppressive conditions (Schlech et al., 1983; Büla et al., 1995). Elderly, pregnant women, neonates, and immunocompromised individuals are particularly susceptible to L. monocytogenes: the number of cases among the elderly population (>64 years) increased from 56% in 2008 to 64% in 2013 (EFSA, 2016). The Center for Disease Control and Prevention in United States (CDC, 2012) emphasizes that people over 50 years, and especially those over 65, should avoid hot dogs, lunch meats, cold cuts, and other delicatessen meats, unless they are “steaming hot” or reheated to 73.9°C (165°F).

Clinical Manifestations

The Listeria species pathogenic to humans and animals are L. monocytogenes, L. ivanovii, and L. seeligeri, although L. monocytogenes is associated with the vast majority of cases of Listeria infection. These species are transmitted mainly through contaminated RTE foods. Listeriosis in humans manifests primarily as septicemia, meningitis, encephalitis, gastrointestinal infection, and abortion (McLauchlin et al., 2004). Other less common manifestations are endocarditis, pericarditis, myocarditis, arteritis, pneumonia, sinusitis, conjunctivitis, ophthalmitis, otitis, joint infection, and skin infection (Seeliger and Jones, 1986; Radostits et al., 1994; Vázquez-Boland et al., 2001). Four different median incubation periods related to clinical manifestations are reported (Goulet et al., 2013): 24 h (range 6–240 h) for gastrointestinal forms; 2 d (range 1–12 d) for bacteremia; 9 d (range 1–14 d) for central nervous system cases; and 27.5 d (range 17–67 d) for pregnancy-related cases.

Healthy Carriers

Many animals are healthy carriers of Listeria bacteria, for example, cows. Husu (1990) isolated L. monocytogenes in feces from 6.7% of 3878 randomly selected dairy cows, representing 240 farms in Finland. The shedding of L. monocytogenes from clinically healthy cows means cattle feces can contaminate milk, dairy products, and carcasses with L. monocytogenes and, thus, may contribute to foodborne listeriosis. Less than 1% of humans could be healthy carriers of L. monocytogenes (Grif et al., 2001).

Infectious Dose

In the 1980s in the United States, Switzerland, and the United Kingdom, analyses of L. monocytogenes levels from unopened packages of RTE foods implicated in listeriosis rendered infectious doses ranging from <10² to 10⁷ colony-forming unit/gram (CFU/g) (McLauchlin, 1996a). In addition, the European Commission (1999) considers that the number of L. monocytogenes bacteria has usually been high (>1000 CFU/g) in food residues obtained from patients. During shelf life, the European legal limit is ≤100 CFU/g in RTE food. With the recent rise of listeriosis among people >60 years within the EU, Gillespie et al. (2009) question this limit and recommend that it be revaluated to protect the immunosuppressed population. In Belgium, 12 persons (at least eight were immunosuppressed) were affected in 2011 due to consumption of hard cheese. The level of contamination of the cheese was <100 CFU L. monocytogenes serovar 1/2a per gram (Yde et al., 2012).

Subtyping of L. monocytogenes

The ability to distinguish accurately between different strains within a bacterial species is a fundamental requirement for epidemiological surveillance and microevolution studies (Cooper and Feil, 2004). Beyond the species or subspecies level, isolates can be further differentiated by subtyping (Wiedmann, 2002). The most widely used phenotypic method is serotyping, either with classic methods (Seeliger and Höhne, 1979) or through PCR (Kérouanton et al., 2010), and is widely used in epidemiological surveillance of human and food isolates. Furthermore, the method has the advantage that results can be compared between different laboratories. In addition, Wiedmann et al. (1997) defined three distinct genetic lineages in accordance with Rasmussen et al. (1995). In 2001 Nadon et al., described the relationships between L. monocytogenes serotypes and genetic lineages. Lineage I contains serotypes 1/2b, 3b, 3c, and 4b, lineage II contains serotypes 1/2a, 1/2c, and 3a, and lineage III contains serotypes 4a and 4c. Thereafter, the designation “lineage” has been used by other researchers and remains unchanged. Thus, lineages are based on serovar (Nho et al., 2015). In the present article, we consider the terms serotype and serovar as equivalent concepts, but what we use depends on which authors we refer to. “Serogroup” is by some authors used as equivalent to serotype and serovar; however, more often “serogroup” includes a number of serovars/serotypes.

Food as a Source of Listeriosis—Historical Aspects

Since the disease listeriosis was first identified, it has been considered an occupational infection among veterinarians, farmers, and butchers or related to regular contact with animals (Sepp and Roy, 1963; Kampelmacher and van Noorle Jansen, 1979). Historically, this disease was typically associated with single cases, such as a person being infected while assisting bovine or ovine partus or during slaughter. However, Seeliger (1955) considered the theory of food infectious disease important, as Listeria could be proved to cause group diseases and epidemics. Due to his intensive work, Seeliger observed the first listeriosis outbreak reported in the world (1949–1957 in Halle, Germany). The suspected sources of infection were raw milk, sour milk, cream, and cottage cheese; ∼100 individuals were implicated, and the human L. monocytogenes isolates belonged to serogroup 1/2 (Seeliger, 1961).

In 1954, an outbreak involving 26 individuals occurred in Jena, Germany, and 1 year later in 1955, an outbreak in 41 neonatals was reported from Prague, Czechoslovakia. The human L. monocytogenes isolates shared serogroup 1/2; however, in both outbreaks, the vehicle of transmission was not identified. In 1956, a correlation between the consumption of pork meat on a Soviet kolkhoz and 19 human cases of listeriosis was suspected (Mencikova, 1956; Kampelmacher, 1962; Ho et al., 1986; McLauchlin et al., 1986; Sutherland et al., 2003).

The possible relationship between human listeriosis and animal products was discussed during the Giessen symposium on listeriosis in West Germany, 1957, although this was based on a description of a few cases with a suspected source of infection. In the second symposium on listeric infection in Montana, United States, 1962, researchers continued to deliberate about potential sources of human listerial infection (e.g., raw milk, egg and egg products, and meat and meat products). Researchers also realized that hygiene in kitchens and food-producing plants could pose a problem and that food products contaminated with Listeria contaminate hands, utensils, and kitchen tables (Kampelmacher, 1962). In the beginning of 1960s, during a possible outbreak of listeriosis in Uppsala, Sweden, bacteriological investigations were undertaken, on for example, eggs and poultry, but no Listeria bacteria were identified (Ekelund et al., 1962): this investigation was two decades before the foodborne route for L. monocytogenes was confirmed. In Yugoslavia in 1974, a study on the survival of L. monocytogenes in white brined cheese made from unpasteurized cow's milk led the authors (Sipka et al., 1974) to recommend the use of only pasteurized milk in the manufacturing of fresh and ripened cheeses.

In Bremen, Germany, two outbreaks occurred as follows: in 1960–1961 (involving 81 individuals) and in 1963 (involving 20 individuals). In 1966, an outbreak of neonatal listeriosis occurred in Halle, East Germany, where 279 individuals were affected, and raw milk was suspected to be the source of infection; the human L. monocytogenes isolates belonged to serovar 1/2a. During the 1970s, three outbreaks were reported in the United States: the first in 1975 involving six neonatals, the second in 1976 among 20 nonpregnant individuals possibly due to raw salad; and the third in 1979, also involving 20 individuals, where raw vegetables and cheese were suspected to be the sources of infection. The human L. monocytogenes isolates in the three American outbreaks belonged to serovar 4b (Seeliger, 1961; Kampelmacher, 1962; Ho et al., 1986; McLauchlin et al., 1986; Sutherland et al., 2003).

Contaminated food as the vehicle for L. monocytogenes infection in humans was finally determined when Schlech et al. (1983) reported an outbreak in Canada in 1981, which was caused by coleslaw salad. Seven nonpregnant individuals and 34 neonatals were implicated; the isolates belonged to serovar 4b. This was an important outbreak, particularly in Northern America as it highlighed that winter-stored cabbage could allow growth of the organism, which originated from manure from infected sheep that had abortions. The several deaths connected with this outbreak alerted the Canadian government to be more vigilant.

Milk- and Cheeseborne Outbreaks 1983–1999

In the United States a further two outbreaks were reported: in Massachusetts 1983 (49 cases), due to pasteurized milk; and, in California 1985 (142 cases), due to soft cheeses; all isolates belonged to serovar 4b (Fleming et al., 1985; Linnan et al., 1988). The soft cheese outbreak was a triggering outbreak for the United States for introducing regulations as L. monocytogenes was considered an adulterant. In Switzerland during 1983–1987, a Swiss soft cheese, Vacherin Mont d'Or, caused 122 cases of listeriosis (Bille and Glauser, 1988; Büla et al., 1995): more than 200 soft cheeses of different brands and types, both domestic and imported, were analyzed for the presence of L. monocytogenes. Among the soft cheeses analyzed, 8–10% harbored L. monocytogenes. However, the only cheese isolates matching the two particular epidemic human strains of L. monocytogenes serovar 4b with two different phage types were found in Vacherin Mont d'Or soft cheese (Bille, 1988; Bille and Glauser, 1988). This cheese was also sold in Sweden, and human isolates of one of the L. monocytogenes molecular subtype from Vacherin Mont d'Or were identified in 47 Swedish patients during 1971–1990 (Lopez-Valladares et al., 2014).

The first diagnosed foodborne outbreak in Denmark occurred in 1985–1987 and involved 35 individuals; the source of infection was associated with milk products, but was not conclusively determined (serovar 4b; Samuelsson et al., 1990; Peter Gerner-Smidt, pers. comm.). In 1987, a sporadic case of listerial meningitis due to heavily contaminated French pasteurized soft country cheese was reported in Britain. The implicated L. monocytogenes subtype was found in a package consumed by the patient and was indistinguishable from the patient's isolate (serovar 4b; Bannister, 1987). A second reported sporadic case in 1988 was associated with the consumption of vacuum-packed fresh goat's cheese (Anari) from an English manufacturer (serovar 4b; McLauchlin et al., 1990). A second Danish outbreak (serovar 4b), occurring during 1989–1990 and involving 26 patients, was identified by Jensen et al. (1994), and there was weak evidence for blue mold cheese (Peter Gerner-Smidt, pers. comm.). In Philadelphia, United States, a listerial outbreak during 1986–1987 involving 36 individuals was investigated. However, L. monocytogenes could not be isolated from food products eaten by the patients, except from Brie cheese eaten by one patient that matched the patient's isolate (Schwartz et al., 1989).

Due to these outbreaks of listeriosis, in 1986, France established the first control measures for cheese-processing manufacturers selling cheeses to the United States. In 1988, after the Swiss cheese outbreak (1983–1987), French authorities expanded the control to cover all cheese-processing plants (Goulet et al., 2001). Milking hygiene was improved, and cows with L. monocytogenes mastitis were not used for milk production. In addition, several precautionary measures in raw milk cheese preparation are in place. French investigators suggest that a substantial part of the decrease in L. monocytogenes in RTE French food, including cheese, is related to control measures implemented at the food production level (De Valk et al., 2000; De Buyser et al., 2001; Sanaa et al., 2004).

In 1989, the English government advised vulnerable people against eating soft cheeses (McLauchlin et al., 1991). Routine surveillance in the United Kingdom revealed that contamination of soft cheeses with L. monocytogenes decreased from 10% in 1987 to 1% in 1995, and even the CFU of L. monocytogenes per gram declined (McLauchlin, 1996b).

However, despite the regulations, outbreaks associated with L. monocytogenes serovar 4b and cheese continued during the 1990s; three outbreaks occurred in France due to the consumption of soft cheeses contaminated with L. monocytogenes serovar 4b. The first documented outbreak was associated with soft raw milk cheese, Brie de Meaux, in 1995 and involved 36 patients. The French National Reference Center at the Pasteur Institute, Paris, isolated the epidemic strain from four samples of Brie de Meaux among 2500 food isolates (Goulet et al., 1995; De Valk et al., 2000; De Buyser et al., 2001). The second outbreak in 1997 was due to the consumption of soft raw milk cheese Pont l'Évêque, Livarot and infected 14 people (Jacquet et al., 1998; De Valk et al., 2000; De Buyser et al., 2001). In a case–control study in Metropolitan France during 1997, 49% of enrolled sporadic cases of listeriosis could be attributed to eating soft cheese: the authors' (De Valk et al., 1998, p. 21) state that “Soft cheese may account for a substantial proportion of sporadic listeriosis”. The third documented outbreak in France that occurred in 1999 involved three listeriosis cases due to the consumption of the soft raw milk cheese Epoisses (serovar 4b, De Buyser et al., 2001).

In Sweden, contaminated French cheeses were identified. During 1989–1993, 13 (43.3%) out of 30 French soft cheeses made of raw milk purchased in Sweden tested positive for L. monocytogenes. The majority of the positive French cheeses harbored serogroup 1/2, but <100 CFU/g L. monocytogenes; however, in the two cheeses with the largest number (2300 and 100,000 CFU/g of L. monocytogenes), the serogroup was 4 (Loncarevic et al., 1995). In 1997, a fatal case of listeriosis associated with the consumption of French Camembert cheese was reported in Belgium; the isolates from both patient and cheese belonged to serovar 1/2a (Gilot et al., 1997).

Other RTE Food Outbreaks 1987–2002

During the late 1980s and the 1990s, not only cheeses but a wide variety of foods especially RTE foods with long shelf life were identified as vehicles for transmission of L. monocytogenes. These included paté (outbreak 1987–1989, serovar 4b, McLauchlin et al., 1991) and pork tongue in aspic (outbreak 1992, serovar 4b, Goulet et al., 1993). In 1992, the French control measure, previously only related to cheese production, was extended to all meat-processing manufacturers in 1992 and was expanded to all foodstuffs possibly contaminated with L. monocytogenes, the year after (Goulet et al., 2001).

During the 1990s, more vehicles of transmission for listeriosis were identified, such as rillettes (outbreak 1993, serovar 4b, Goulet et al., 1998) and salad with corn and tuna (outbreak 1997, serovar 4b, Aureli et al., 2000). In the 1990s, the first outbreaks caused by cold-smoked rainbow trout (1994–1995, Sweden, serovar 4b and 1999, Finland, serovar 1/2a) were reported (Ericsson et al., 1997: Miettinen et al., 1999). In 1998–1999, a multistate outbreak of listeriosis in the United States was associated with contaminated hot dogs and was caused by a strain of L. monocytogenes serovar 4b. In 2002, another multistate outbreak of listeriosis also involved bacteria of serotype 4b and was attributed to contaminated turkey deli meats (Kathariou et al., 2006; Mead et al., 2006). In 1999–2000, two L. monocytogenes serovar 4b outbreaks occurred in France due to rillettes (10 cases) and pork tongue in aspic (32 cases) (De Valk et al., 2001).

Shift of Serovars

During the1970s, 1980s, and 1990s, the majority of human cases of listeriosis worldwide were linked to lineage I, serovar 4b (Orsi et al., 2011; Lopez-Valladares et al., 2014). A majority of foodborne listeriosis outbreaks appear to have been caused by serovar 4b (Kathariou, 2002). In 1987, 59% of 722 cases of listeriosis in Britain were due to L. monocytogenes serovar 4b (McLauchlin, 1987), and in 1991, serovar 4b prevailed in human listeriosis in most of Europe, with serovar 4b accounting for 63.9% in France and 64% in United Kingdom (Farber and Peterkin, 1991). The dominance of serovar 4b in human listeriosis was reported from England, Wales and Northern Ireland, 1983–1992 (McLauchlin and Newton, 1995); The Netherlands, 1976–1995 and 1999–2003 (Aouaj et al., 2002; Doorduyn et al., 2006); Spain, 1989–1998 (Vela et al., 2001); Portugal, 1994–2007 (Almeida et al., 2006, 2010) and 2008–2012 (Magalhães et al., 2014); and Japan, 1991 (Nakama et al., 1998). During 1990–1999, serovar 4b dominated (52.0%) among human strains in different regions in Italy, whereas serovar 1/2a constituted only 27.2% (Gianfranceschi et al., 2003).

In the middle of 1990s and the early 2000s, a shift from L. monocytogenes serovar 4b to serovar 1/2a causing human listeriosis occurred, and serovar 1/2a became more frequently linked to outbreaks of listeriosis, particularly in Europe and North America.

During an international Listeria conference (ISOPOL) in Australia 1995, Gerner-Smidt et al. (1995) report that until 1992 in Denmark, two-thirds of human L. monocytogenes isolates belonged to serogroup 4; the following year, 1993, serogroup 1 ( = 1/2) became predominant in Denmark. Similar results were reported from United Kingdom at the same conference. The conclusion in the conference report abstract from the United Kingdom states, “The trends towards an increase in listeriosis amongst the immunocompromised, together with the increase in cases due to serogroup 1/2, mean that future resources will be directed at improving our ability to subtype within serogroup 1/2” (McLauchlin and Newton, 1995).

Orsi et al. (2011) stress that lineage II, serotype 1/2a strains appear more common among human listeriosis cases in Northern Europe, which is confirmed by Rosef et al. (2012) from Norway, where 55.6% of human clinical isolates collected between 1992 and 2005 were lineage II and 41.6% were lineage I with ribotyping. The change in the serotypes of human L. monocytogenes isolates is observed in Finland in L. monocytogenes isolates from invasive infections during an 11-year period, 1990–2001. Since 1990, the number of cases caused by serotype 4b in Finland has remained constant, with some exceptions. However, the number of listeriosis cases caused by serovar 1/2a increased between 1990 and 2001 and has exceeded the number of cases caused by serovar 4b since 1991 (Lukinmaa et al., 2003). Even during 2002–2004, serovar 1/2a was predominant in Finland (Lyytikäinen et al., 2006). In Denmark, during 2002–2012, 42% of human isolates belonged to lineage I and 58% to lineage II: the lineage II isolates belonged to serotype 1, predominantly serovar 1/2a, as determined by PCR (Jensen et al., 2016a).

Between 1972 and 1995, human listeriosis in Sweden was mainly caused by serovar 4b. However, since 1996, serovar 1/2a has been the dominant L. monocytogenes serovar in human listeriosis in Sweden (Lopez-Valladares et al., 2014): the changes in serogroup distribution among human cases in Sweden might be explained by changes in eating habits (Loncarevic et al., 1998). Other countries also report L. monocytogenes serovar 1/2a to be dominant in human listeriosis: Germany, 2001–2005 (Koch and Stark, 2006); Italy, Lombardy, and Tuscany regions, 1996–2007 (Mammina et al., 2009), and Lombardy region, 2006–2010 (Mammina et al., 2013).

Mammina et al. (2013) suggest that serotype 1/2a has replaced serotype 4b worldwide as the leading serotype causing human listeriosis, as human L. monocytogenes isolates collected in Italy during 2000–2010 were 46.6% serovar 1/2a and 30.7% serovar 4b (Pontello et al., 2012). Bertrand et al. (2016, p. 1/16) observe an increase among nonpregnant cases in Belgium “probably due to the rise of highly susceptible patients in an aging population…“and”…can be attributed to significant increase in incidence of isolates belonging to serovar 1/2a.” The shift from serovar 4b to 1/2a is also seen in Switzerland, serogroup 1/2 became predominant among human strains after 1994 (Pak et al., 2002), and during 2011–2013, the number of human isolates of serovar 1/2a was more than twice the number of 4b isolates (Althaus et al., 2014). In Canada, between 1995 and 2004, serotype 1/2a was the predominant serotype among human cases, with serotype 4b being predominant in cases associated with pregnancy and miscarriage. Among 722 human isolates, serovar 1/2a (47.5%) and serovar 4b (30.0%) were identified (Clark et al., 2010). In the Czech Republic during 2013–2016, 58% of human listeriosis cases were caused by serovar 1/2a; serovar 4b accounted for only 28.6% (Gelbicova et al., 2017).

Large outbreaks of listeriosis predominantly caused by serogroup 4b strains have become less frequent (Swaminathan and Gerner-Smidt, 2007). Lomonaco et al. (2015, p. 176) state that “an apparent shift has been observed in the last ten years, as serotype 1/2a is the one being more frequently linked to outbreaks of listeriosis, particularly in Europe and North America.” Swaminathan and Gerner-Smidt (2007) claim that blood stream infection (BSI) is now a more common clinical presentation in listeriosis than meningoencephalitis, and serovars 1/2a and 1/2b are more common in BSIs than in meningoencephalitis. Thus, more BSI may lead to more serovar 1/2a and 1/2b in listeriosis. “…the chance a blood stream infection will be detected has increased because the blood culturing systems have become more sensitive and the indications for drawing a blood culture have become broader in the past 20 years.…” (Swaminathan and Gerner-Smidt, 2007, p. 1242). In Denmark, Jensen et al. (2016a) also report an increase in BSIs among patients >60 years old, and during 2005–2009, lineage II isolates were the main cause of the increase. A simple reason for more 1/2a cases of listeriosis may be due to the frequent occurrence of this serovar in increasingly popular RTE foods (Gilbreth et al., 2005). A link between serovar 1/2a isolates obtained from patients and isolates obtained from smoked fish is reported in Scandinavian countries (Sweden, Norway, and Finland) and in eastern Spain (Luber et al., 2011; Ariza-Miguel et al., 2015).

Reported Outbreaks Caused by L. monocytogenes 1/2a Since 2000

Since 2000, several L. monocytogenes 1/2a outbreaks have been reported. Sliced processed delicatessen turkey meat caused 30 listeriosis cases in 2000 in the United States (Olsen et al., 2005). Flat whipping cream caused an outbreak, including at least five individuals in Canada in 2001 (Pagotto et al., 2006; Clark et al., 2010). Fresh cheeses made of raw goat and cow milk caused a gastrointestinal outbreak among 120 individuals in Sweden in 2001 (Danielsson-Tham, 2004). In 2001, in Los Angeles County, United States, 16 cases suffered from acute febrile gastroenteritis due to leftover turkey (Frye et al., 2002).

Sandwiches collected from a hospital and external sandwich producer in the United Kingdom infected two patients in 2003 (Shetty et al., 2009). In the Swindon area, United Kingdom during autumn 2003, five cases in one particular hospital were due to prepacked sandwiches from a retail outlet (Dawson et al., 2006). In 2005, a small cheese outbreak involving 10 individuals occurred in Switzerland; the implicated soft cheese, known as tomme cheese, was produced by a local manufacturer (Bille et al., 2006).

In 2007, 17 patients were possibly infected by Camembert cheese produced at a small Norwegian dairy (Johnsen et al., 2010). In 2008 in New York City, United States, five patients in a hospital suffered from listeriosis due to tuna salad prepared in the hospital (Cokes et al., 2011). Multiprovince outbreaks occurred in Canada in 2008 and involved 57 cases due to delicatessen meat (Currie et al., 2015) and 38 cases due to soft washed-rind cheese (Gaulin et al., 2012).

In Denmark in 2009, seven patients in a hospital had received a meal with beef from the same meals-on-wheels delivery catering company (Smith et al., 2011). In 2009–2010, a multinational outbreak occurred in Germany, Austria, and the Czech Republic and involved 34 cases. The implicated red-smear cheese (Quargel) was produced in Austria, and these cheeses were distributed to Poland and Slovakia (Fretz et al., 2010). A major listeriosis outbreak involving 43 patients in Northern Italy was linked to soft cheese (Taleggio cheese) in 2009–2011 (Amato et al., 2017). In 2010, precut celery caused 10 cases in a hospital in Texas, United States (Gaul et al., 2013). A multistate outbreak in United States, due to Cantaloupe, infected 146 persons in 2011. Five subtypes of L. monocytogenes were involved and shared serovar 1/2a and 1/2b (Laksanalamai et al., 2012).

In 2011, there were outbreaks, including 12 patients in Belgium, possibly due to hard cheese (Yde et al., 2012), and six cases in Switzerland, due to cooked ham (Hachler et al., 2013). Intact packages of imported soft salty cheese (ricotta salata) made from pasteurized sheep milk yielded a multistate outbreak in United States in 2012 involving 22 cases (Heiman et al., 2016). Two cases in Bizkaia, Spain, in 2012 were associated with the consumption of Latin-style fresh cheese made in Portugal from pasteurized milk (De Castro et al., 2012).

In municipal hospital wards in Finland, 12 cases were reported in 2012 due to ready-sliced meat jelly (Jacks et al., 2016). A protracted outbreak in Germany in 2012–2016 involved 57 human cases and was due to smoked pork belly (Kleta et al., 2017). A community outbreak involving three cases in Scotland in 2013 was due to RTE meat (Okpo et al., 2015). In Sweden 2013–2014, 51 patients were affected due to cold cuts (Dahl et al., 2017). A hospital-acquired outbreak during 2014–2015 in Washington State, United States, was linked to milkshakes (Li et al., 2017).

Reported Outbreaks Caused by L. monocytogenes 1/2b and 4b Since 2000

Outbreaks due to lineage I, serovar 1/2b and 4b have also occurred:

Soft cheese (Mexican style) contaminated by serovar 4b caused 13 cases in the United States in 2000 (MacDonald et al., 2005). In 2001 in Japan, 86 people were infected by serovar 1/2b after the consumption of washed-type cheese: this was the first documented incidence of foodborne listeriosis in Japan (Makino et al., 2005). In 2002, turkey deli meat, serovar 4b infected 54 cases in nine U.S. states (Gottlieb et al., 2006). In British Columbia, Canada, soft ripened cheese caused 134 foodborne cases of listeriosis during two separate listeriosis outbreaks in 2002 and was due to serovar 4b (McIntyre et al., 2015). In 2006–2007, a large listeriosis outbreak (189 cases) occurred in Germany due to the consumption of acid curd soft cheese made from pasteurized milk and ripened with a red smear: it was contaminated with serovar 4b (Koch et al., 2010). A cohort study in Austria revealed a serovar 4b outbreak of gastroenteritis in 2008 among 16 persons who had eaten mixed cold cuts (including jellied pork) at a wine tavern (Pichler et al., 2009).

A retrospective study detected a listeriosis outbreak, involving 30 individuals, in Portugal between 2009 and 2012. This was due to the consumption of cheese (queijo fresco) from cow and goat pasteurized milk and belonged to serogroup IVb (Magalhães et al., 2015). In England, 14 people were affected between 2010 and 2012 due to the consumption of pork pies associated with the process of adding gelatin to the pies after cooking; the outbreak was due to serovar 4b (Awofisayo-Okuyelu et al., 2016). In 2013, a multistate outbreak of listeriosis (five cases) in the United States was linked to soft-ripened cheese and was due to serovar 4b (Choi et al., 2014). In 2013–2014, there were 32 cases of listeriosis infected with serovar 4b in Switzerland: RTE salads were the vehicle (Stephan et al., 2015). RTE spiced meat roll from a single production facility caused an outbreak in Denmark in 2014 involving 41 cases and due to serogroup IIb (Jensen et al., 2016b). Frequently occurring outbreaks due to Mexican-style cheeses are usually caused by serovar 4b (Cartwright et al., 2013).

Vaccum-Packed Gravad and Smoked Fish

Vacuum-packed gravad and smoked fish are still the most frequently L. monocytogenes–contaminated RTE foods (EFSA, 2011). L. monocytogenes has been isolated from gravad, hot and cold-smoked rainbow trout (Oncorhynchus mykiss), and salmon (Salmo salar) around the world. Løvdal (2015) summarizes results from scientific publications from 2000 and highlights a prevalence of L. monocytogenes in the retail sector of 0–61%, for cold-smoked salmon, with an average of 9.8%. The serovar most often encountered in these products is serovar 1/2a (Lopez-Valladares et al., 2014). Gravad and cold-smoked salmon are vacuum-packed RTE products with a generous best before date of normally 4–5 weeks and constitute an optimal environment for the facultative anaerobic, psychrotrophic organism Listeria. In the Scandinavian countries, RTE vacuum-packed fish products are popular foods (Lukinmaa et al., 2003; Jensen et al., 2016a), and during the 1990s, outbreaks of listeriosis occurred in Sweden due to rainbow trout (Ericsson et al., 1997) and in Finland due to salmon (Miettinen et al., 1999).

During 2013–2015, two outbreaks involving 20 cases occurred in Denmark and were associated with cold-smoked or gravad fish products. All cases belonged to known risk groups, and the two epidemic strains involved were serotype IIa (Lassen et al., 2016). During the same period, an outbreak (serovar 1/2a) in Sweden involved 27 clinical cases and was due to gravad and smoked fish products produced by one manufacturer (Lopez-Valladares G., pers. comm.).

One reason for few fish-borne outbreaks being reported could be that the long incubation period for listeriosis renders it difficult to determine the food source (Tompkin, 2002). Another theory why outbreaks due to fish consumption are rare is presented by Rocourt et al. (2000): as factories producing fish products are often smaller than factories processing milk and meat products, fewer people will be affected if fish products are contaminated. Conversely, smaller outbreaks are being identified more than in the1980s and 1990s. One reason may be more optimal detection methods and new characterization methods that generate DNA sequences (Buchanan et al., 2017).

The number of invasive listeriosis cases due to cold-smoked salmon consumption in France is predicted to be 307 per year. Even if this calculation is uncertain, it is based on scientific observations and can be used to manage the risk linked to the consumption of contaminated cold-smoked salmon (Pouillot et al., 2009).

Africa and Asia

In most African countries and also in many Asian countries, Listeria research is in its infancy.

There are studies reporting the prevalence of L. monocytogenes in food in Africa and Asia. However, understanding of the relationships with the disease is hampered by the lack of surveillance of listeriosis (Chen et al., 2009; Paudyal et al., 2017; Amajoud et al., 2018).

In many traditional Asian cuisines, such as in Vietnam, raw products are seldom consumed, processed food is not approachable, and most food is cooked just before consumption. However, change in dietary habits in developing countries may give rise to changes in foodborne infections, and change in life expectancy, disease patterns, and more people taking, for example, proton pump inhibitors may render the population more susceptible to Listeria infection (Tran et al., 2010).

Concluding Remarks

Listeriosis is still a topical foodborne disease. The world's population is aging and has a greater chance of developing debilitating chronic conditions. The demographic shift and the widespread use of immunosuppressive medications have increased the immunocompromised population that are susceptible to an increased risk for listeriosis (Allerberger and Wagner, 2010; Luber et al., 2011; Todd and Notermans, 2011).

Consumer lifestyle has changed, and less time is available for food preparation. Modern lifestyle has markedly changed eating habits worldwide, with a consequent increased demand for RTE foods (De Oliveira et al., 2010); therefore, more RTE and takeaway foods are consumed. Within the food industry, extended shelf life RTE foods and new RTE food types are an area of expansion, and as these foods pose the most concern for listeriosis, this area deserves more attention (Allerberger and Wagner, 2010). To be able to control L. monocytogenes in RTE products at risk, these products should be properly labeled with regard to time and temperature of storage, and consumers should be educated about food storage practices. In addition, the shelf life for some products with a known risk of L. monocytogenes contamination and growth (e.g., vacuum-packed gravad and cold-smoked salmon) should be restricted by authority regulations.

There is a concern that many Listeria outbreaks are reported from hospitals. Even low levels of L. monocytogenes pose a risk to immunocompromised people, and RTE food is often served in hospitals. In the United Kingdom, it is recommended that food served to hospital patients is free from L. monocytogenes (Fretz et al., 2010; Coetzee et al., 2011; Yde et al., 2012). Large-scale delivery of precooked meals to a vulnerable population represents a threat if proper measures against listeriosis are not taken (Smith et al., 2011). We consider that it is vitally important that foods (especially cooked and chilled) delivered to hospitals and residential homes for senior citizens and elderly people are reheated to at least 72°C and that cold food, such as turkey deli meat and cold-smoked and gravad salmon, should be free from L. monocytogenes.

Footnotes

Disclosure Statement

No competing financial interests exist.

References

Allerberger

, Wagner

. Listeriosis: A resurgent foodborne infection. Clin Microbiol Infect, 2010; 16:16–23.

Almeida

, Morvan

, Magalhães

, Santos

, Hogg

, Leclercq

, Teixeira

, Research

Team

. Distribution and characterization of Listeria monocytogenes clinical isolates in Portugal, 1994–2007. Eur J Cin Microbiol Infect Dis, 2010; 29:1219–1227.

Almeida

, Gibbs

, Hogg

, Teixeira

. Listeriosis in Portugal: An existing but under reported infection. BMC Infect Dis, 2006; 6:153.

Althaus

, Lehner

, Brisse

, Maury

, Tasara

, Stephan

. Characterization of Listeria monocytogenes strains isolated during 2011–2013 from human infections in Switzerland. Foodborne Pathog Dis, 2014; 11:753–758.

Amajoud

, Leclercq

, Soriano

, Bracq-Dieye

, El Maadoudi

, Senhaji

, Kounnoun

, Moura

, Lecuit

, Abrini

. Prevalence of Listeria spp. and characterization of Listeria monocytogenes isolated from food products in Tetouan, Morocco. Food Control, 2018; 84:436–441.

Amato

, Filipello

, Gori

, Lomonaco

, Losio

, Parisi

, Huedo

, Knabel

, Pontello

. Identification of a major Listeria monocytogenes outbreak clone linked to soft cheese in Northern Italy 2009–2011. BMC Infect Dis, 2017; 17:342.

Aouaj

, Spanjaard

, van Leeuwen

, Dankert

. Listeria monocytogenes meningitis: Serotype distribution and patient characteristics in The Netherlands, 1976–1995. Epidemiol Infect, 2002; 128:405–409.

Ariza-Miguel

, Fernández-Natal

, Soriano

, Hernández

, Stessl

, Rodríguez-Lázaro

. Molecular epidemiology of invasive listeriosis due to Listeria monocytogenes in a Spanish hospital over a nine-year study period, 2006–2014. BioMed Res Int, 2015; 2015:191409.

Aureli

, Fiorucci

, Caroli

, Marchiaro

, Novara

, Leone

, Salmaso

. An outbreak of febrile gastroenteritis associated with corn contaminated by Listeria monocytogenes . N Engl J Med, 2000; 342:1236–1241.

10.

Awofisayo-Okuyelu

, Arunachalam

, Dallman

, Grant

, Aird

, McLauchlin

, Painset

, Amar

. An outbreak of human listeriosis in England between 2010 and 2012 associated with the consumption of pork pies. J Food Prot, 2016; 79:732–740.

11.

Baka

, Noriega

, Tsakali

, Van Impe

JFM

. Influence of composition and processing of Frankfurter sausages on the growth dynamics of Listeria monocytogenes under vacuum. Food Res Int, 2015; 70:94–100.

12.

Bannister

BA.

Listeria monocytogenes meningitis associated with eating soft cheese. J Infect, 1987; 15:165–168.

13.

Bertrand

, Ceyssens

, Yde

, Dierick

, Boyen

, Vanderpas

, Vanhoof

, Mattheus

. Diversity of Listeria monocytogenes strains of clinical and food chain origins in Belgium between 1985 and 2014. PLoS One, 2016; 11:e0164283.

14.

Bille

. Anatomy of a foodborne listeriosis outbreak. In: Foodborne Listeriosis. Proceedings of a Symposium, September 7, 1988. Wiesbaden

FRG

. Hamburg, Germany: Behr's Verlag GmBH, 1988, pp. 31–36.

15.

Bille

, Blanc

, Schmid

, Boubaker

, Baumgartner

, Siegrist

, Tritten

, Lienhard

, Berner

, Anderau

, Treboux

, Ducommun

, Malinverni

, Genné

, Erard

, Waespi

. Outbreak of human listeriosis associated with tomme cheese in northwest Switzerland, 2005. Euro Surveill, 2006; 11:91–93.

16.

Bille

, Glauser

. Listériose en Suisse. [The situation of listeriosis in Switzerland]. Bull des Bundessamtes für Gesundheitswesen, 1988; 3:28–29.

17.

Buchanan

, Gorris

LGM

, Hayman

, Jackson

, Whiting

. A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control, 2017; 75:1–13.

18.

Büla

, Bille

, Glauser

. An epidemic of food-borne listeriosis in western Switzerland: Description of 57 cases involving adults. Clin Infect Dis, 1995; 20:66–72.

19.

Cartwright

, Jackson

, Johnson

, Graves

, Silk

, Mahon

. Listeriosis outbreaks and associated food vehicles, United States, 1998–2008. Emerg Infect Dis, 2013; 19:1–9.

20.

[CDC] Center for Disease Control and Prevention in the United States. Listeria (Listeriosis)—Prevention. 2012. Available at: www.cdc.gov/listeria/prevention.html, accessed December 21, 2017 .

21.

Chen

, Zhang

, Mei

, Jiang

, Fang

. Prevalence of Listeria in Chinese food products from 13 provinces between 2000 and 2007 and virulence characterization of Listeria monocytogenes isolates. Foodborne Pathog Dis, 2009; 6:7–14.

22.

Choi

, Jackson

, Medus

, Beal

, Rigdon

, Cloyd

, Forstner

, Ball

, Bosch

, Bottichio

, Cantu

, Melka

, Ishow

, Slette

, Irvin

, Wise

, Tarr

, Mahon

, Smith

, Silk

. Multistate outbreak of listeriosis linked to soft-ripened cheese—United States, 2013. MMWR, 2014; 63:294–295.

23.

Clark

, Farber

, Pagotto

, Ciampa

, Dore

, Nadon

, Bernard

, Ng

. Surveillance for Listeria monocytogenes and listeriosis, 1995–2004. Epidemiol Infect, 2010; 138:559–572.

24.

Coetzee

, Laza-Stanca

, Orendi

, Harvey

, Elviss

, Grant

. A cluster of Listeria monocytogenes infections in hospitalised adults, Midlands, England, February 2011. Euro Surveill, 2011; 16:pii19869.

25.

Cokes

, France

, Reddy

, Hanson

, Lee

, Kornstein

, Stavinsky

, Balter

. Serving high-risk foods in a high-risk setting: Survey of hospital food service practices after an outbreak of listeriosis in a hospital. Infect Control Hosp Epidemiol, 2011; 32:380–386.

26.

Cooper

., Feil

. Multilocus sequence typing—what is resolved?. Trends Microbiol, 2004; 12:373–377.

27.

Currie

, Farber

, Nadon

, Sharma

, Whitfield

, Gaulin

, Galanis

, Bekal

, Flint

, Tschetter

, Pagotto

, Lee

, Jamieson

, Badiani

, MacDonald

, Ellis

, May-Hadford

, McCormick

, Savelli

, Middleton

, Allen

, Tremblay

, MacDougall

, Hoang

, Shyng

, Everett

, Chui

, Louie

, Bangura

, Levett

, Wilkinson

, Wylie

, Reid

, Major

, Engel

, Douey

, Huszczynski

, Di Lecci

, Strazds

, Rousseau

, Ma

, Isaac

, Sierpinska

. Multi-province listeriosis outbreak linked to contaminated deli meat consumed primarily in institutional settings, Canada, 2008. Foodborne Pathog Dis, 2015; 12:645–652.

28.

Dahl

, Sundqvist

, Hedenström

, Löfdahl

, Alm

, Ringberg

, Lindblad

, Wallensten

, Thisted

, Jernberg

. A nationwide outbreak of listeriosis associated with cold-cuts, Sweden 2013–2014. Infect Ecol Epidemiol, 2017; 7:1324232.

29.

Danielsson-Tham

, Ericsson

, Helmersson

, Leffler

, Lüdtke

, Steen

, Sørgjerd

, Tham

. Causes behind a human cheese-borne outbreak of gastrointestinal listeriosis. Foodborne Pathog Dis, 2004; 1:153–159.

30.

Dawson

, Evans

, Willby

, Bardwell

, Chamberlain

, Lewis

. Listeria outbreak associated with sandwich consumption from a hospital retail shop, United Kingdom. Euro Surveill, 2006; 11:89–91.

31.

De Buyser

, Dufour

, Maire

, Lafarge

. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol, 2001; 67:1–17.

32.

De Castro

, Escudero

, Rodriguez

, Muniozguren

, Uribarri

, Saez

, Vazquez

. Listeriosis outbreak caused by latin-style fresh cheese, Bizkaia, Spain, August 2012. Euro Surveill, 2012; 17:8–10.

33.

De Oliveira

, Ribeiro

EGA

, Bergamini

AMM

, De Martinis

ECP

. Quantification of Listeria monocytogenes in minimally processed leafy vegetables using a combined method based on enrichment and 16S rRNA real-time PCR. Food Microbiol, 2010; 27:19–23.

34.

De Valk

, Vaillant

, Goulet

, Henrion

. [The epidemiology of human listeriosis in France]. Epidémiology des listérioses humaines en France. Bull Acad National Med, 2000; 184:267–274.

35.

De Valk

, Vaillant

, Jacquet

, Rocourt

, Le Querrec

, Stainer

, Quelquejeu

, Pierre

, Desenclos

, Goulet

. Two consecutive nationwide outbreaks of listeriosis in France, October 1999–February 2000. Am J Epidemiol, 2001; 154:944–950.

36.

De Valk

, Vaillant

, Pierre

, Rocourt

, Jacquet

, Lequerrec

, Thomas

, Goulet

. Risk factors for sporadic listeriosis in France. In: Program and Abstracts XIII International Symposium on Problems of Listeriosis. Halifax, Nova Scotia, Canada, June 28–July 2, 1998, p. 21.

37.

Doorduyn

, de Jager

, van der Zwaluw

, Wannet

WJB

, van der Ende

, Spanjaard

, Van Duynhoven

YTHP

. Invasive Listeria monocytogenes infections in the Netherlands, 1995–2003. Euro J Clin Microbiol Infect Dis, 2006; 25:433–442.

38.

EFSA (European Food Safety Authority). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA J, 2011; 9:2090, 378 pp.

39.

EFSA (European Food Safety Authority). Zoonoses Report: Listeria Infections Stable but Frequently Reported Among the Elderly. 2016. Available at: www.efsa.europa.eu/en/press/news/161216, accessed November 1, 2017 .

40.

Ekelund

, Laurell

, Melander

, Olding

, Vahlquist

. Listeria infection in the foetus and the newborn: A clinical, pathological and epidemiological study. Acta Paediatr, 1962; 51:698–711.

41.

Ericsson

, Eklöw

, Danielsson-Tham

, Loncarevic

, Mentzing

, Persson

, Unnerstad

, Tham

. An outbreak of listeriosis suspected to have been caused by rainbow trout. J Clin Microbiol, 1997; 35:2904–2907.

42.

European Commission. Health and Consumer Protection Directorate-General. Directorate B–Scientific Health Opinions. Unit B3–Management of scientific committees II. Opinion of the Scientific Committee on Veterinary Measures Relating to Public Health on Listeria monocytogenes . 1999. Available at: https://ec.europa.eu/food/sites/food/files/safety/docs/sci-com_scv_out25_en.pdf, accessed February 17, 2018 , 44 pp.

43.

Farber

, Peterkin

. Listeria monocytogenes, a food-borne pathogen. Microbiol Mol Biol Rev, 1991; 55:476–511.

44.

Fleming

, Cochi

, MacDonald

, Brondum

, Hayes

, Plikaytis

, Holmes

, Audurier

, Broome

, Reingold

. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med, 1985; 312:404–407.

45.

Fretz

, Pichler

, Sagel

, Much

, Ruppitsch

, Pietzka

, Stöger

, Huhulescu

, Heuberger

, Appl

, Werber

, Stark

, Prager

, Flieger

, Karpíšková

, Pfaff

, Allerberger

. Update: Multinational listeriosis outbreak due to ‘Quargel’, a sour milk curd cheese, caused by two different L. monocytogenes serotype 1/2a strains, 2009–2010. Euro Surveill, 2010; 15:2–3.

46.

Frye

, Zweig

, Sturgeon

, Tormey

, LeCavalier

, Lee

, Lawani

, Mascola

. An outbreak of febrile gastroenteritis associated with delicatessen meat contaminated with Listeria monocytogenes . Clin Infect Dis, 2002; 35:943–949.

47.

Gaul

, Farag

, Shim

, Kingsley

, Silk

, Hyytia-Trees

. Hospital-acquired listeriosis outbreak caused by contaminated diced celery—Texas, 2010. Clin Infect Dis, 2013; 56:20–26.

48.

Gaulin

, Ramsay

, Bekal

. Widespread listeriosis outbreak attributable to pasteurized cheese, which led to extensive cross-contamination affecting cheese retailers, Quebec, Canada, 2008. J Food Prot, 2012; 75:71–78.

49.

Gelbicova

, Tomastikova

, Karpiskova

. Molecular-epidemiological characteristics and diversity of Listeria monocytogenes in the human population in the Czech Republic in 2013–2016. Epidemiol Microbiol Immunol, 2017; 66:146–148.

50.

Gerner-Smidt

, Weischer

, Jensen

, Frederiksen

. Listeriosis in Denmark—results of a 10-year survey. In: Proceedings of the XII International Symposium on Problems of Listeriosis, Perth, Western Australia, October 2–6, 1995, p. 472.

51.

Gianfranceschi

, Gattuso

, Tartaro

, Aureli

. Incidence of Listeria monocytogenes in food and environmental samples in Italy between 1990 and 1999: Serotype distribution in food, environmental and clinical samples. Euro J Epidemiol, 2003; 18:1001–1006.

52.

Gilbreth

, Call

, Wallace

, Scott

, Chen

, Luchansky

. Relatedness of Listeria monocytogenes isolates recovered from selected ready-to-eat foods and listeriosis patients in the United States. Appl Environ Microbiol, 2005; 71:8115–8122.

53.

Gillespie

, McLauchlin

, Little

, Penman

, Mook

, Grant

, O'Brien

. Disease presentation in relation to infection foci for non-pregnancy-associated human listeriosis in England and Wales, 2001 to 2007. J Clin Microbiol, 2009; 47:3301–3307.

54.

Gilot

, Hermans

, Yde

, Gigi

, Janssens

, Genicot

, André

, Wauters

. Sporadic case of listeriosis associated with the consumption of a Listeria monocytogenes-contaminated ‘Camembert’ cheese. J Infect, 1997; 35:195–197.

55.

Gottlieb

, Newbern

, Griffin

, Graves

, Hoekstra

, Baker

, Hunter

, Holt

, Ramsey

, Head

, Levine

, Johnson

, Schoonmaker-Bopp

, Reddy

, Kornstein

, Gerwel

, Nsubuga

, Edwards

, Stonecipher

, Hurd

, Austin

, Jefferson

, Young

, Hise

, Chernak

, Sobel

. Multistate outbreak of listeriosis linked to Turkey deli meat and subsequent changes in US regulatory policy. Clin Infect Dis, 2006; 42:29–36.

56.

Goulet

, De Valk

, Pierre

, Stainer

, Rocourt

, Vaillant

, Jacquet

, Desenclos

. Effect of prevention measures on incidence of human listeriosis, France, 1987–1997. Emerg Infect Dis, 2001; 7:983–989.

57.

Goulet

, Jacquet

, Vaillant

, Rebière

, Mouret

, Lorente

, Maillot

, Stainer

, Rocourt

. Listeriosis from consumption of raw-milk cheese. Lancet, 1995; 345:1581–1582.

58.

Goulet

, King

, Vaillant

, De Valk

. What is the incubation period for listeriosis?. BMC Infect Dis, 2013; 13:11.

59.

Goulet

, Lepoutre

, Rocourt

, Courtieu

, Dehaumont

, Veit

. [Epidemic listeriosis in France: Final assessment and results of the epidemiological survey]. Épidémie de listériose en France. Bilan final et resultats de l'enquête épidémiologique. Bull Épidémiol Hebdomadaire, 1993; 13–14.

60.

Goulet

, Rocourt

, Rebiere

, Jacquet

, Moyse

, Dehaumont

, Salvat

, Veit

. Listeriosis outbreak associated with the consumption of rillettes in France in 1993. J Infect Dis, 1998; 177:155–160.

61.

Grif

, Hein

, Wagner

, Brandl

, Mpamugo

, McLauchlin

, Dierich

, Allerberger

. Prevalence and characterization of Listeria monocytogenes in the feces of healthy Austrians. Wiener Klin Wochensch, 2001; 113:737–742.

62.

Hachler

, Marti

, Giannini

, Lehner

, Jost

, Beck

, Weiss

, Bally

, Jermini

, Stephan

, Baumgartner

. Outbreak of listerosis due to imported cooked ham, Switzerland 2011. Euro Surveill, 2013; 18:7–13.

63.

Heiman

, Garalde

, Gronostaj

, Jackson

, Beam

, Joseph

, Saupe

, Ricotta

, Waechter

, Wellman

, Adams-Cameron

, Ray

, Fields

, Chen

, Datta

, Burall

, Sabol

, Kucerova

, Trees

, Metz

, Leblanc

, Lance

, Griffin

, Tauxe

, Silk

. Multistate outbreak of listeriosis caused by imported cheese and evidence of cross-contamination of other cheeses, USA, 2012. Epidemiol Infect, 2016; 144:2698–2708.

64.

, Shands

, Friedland

, Eckind

, Fraser

. An outbreak of type-4b Listeria monocytogenes infection involving patients from eight Boston hospitals. Arch Int Med, 1986; 146:520–524.

65.

Husu

. Epidemiologic studies on the occurrence of Listeria monocytogenes in the feces of dairy-cattle. Zentralbl Veterinarmed B, 1990; 37:276–282.

66.

Jacks

, Pihlajasaari

, Vahe

, Myntti

, Kaukoranta

, Elomaa

, Salmenlinna

, Rantala

, Lahti

, Huusko

, Kuusi

, Siitonen

, Rimhanen-Finne

. Outbreak of hospital-acquired gastroenteritis and invasive infection caused by Listeria monocytogenes, Finland, 2012. Epidemiol Infect, 2016; 144: 2732–2742.

67.

Jacquet

, Saint-Cloment

, Brouille

, Catimel

, Rocourt

. [Human listeriosis in France in 1997]. La listeriose humaine en France en 1997. Données du Centre National de Reference des Listeria . Bull Épidémiol Hebdomadaire, 1998; 33:142–143.

68.

Jensen

, Frederiksen

, Gerner-Smidt

. Risk factors for listeriosis in Denmark, 1989–1990. Scand J Infect Dis, 1994; 26:171–178.

69.

Jensen

, Björkman

, Ethelberg

, Kiil

, Kemp

, Møller Nielsen

. Molecular typing and epidemiology of human listeriosis cases, Denmark, 2002–2012. Emerg Infect Dis, 2016a;22:625–633.

70.

Jensen

, Nielsen

, Bjorkman

, Jensen

, Muller

, Persson

, Bjerager

, Perge

, Krause

, Kiil

, Sørensen

, Andersen

, Molbak

, Ethelberg

. Whole-genome sequencing used to investigate a nationwide outbreak of listeriosis caused by ready-to-eat delicatessen meat, Denmark, 2014. Clin Infect Dis, 2016b;63:64–78.

71.

Johnsen

, Lingaas

, Torfoss

, Strøm

, Nordøy

. A large outbreak of Listeria monocytogenes infection with short incubation period in a tertiary care hospital. J Infect, 2010; 61:465–470.

72.

Kampelmacher

. Animal products as a source of listeric infection in man. In: Proceedings of the Second International Symposium on Listeric Infection. Gray

(ed.). Bozeman, MN: Montana State College, 1962, pp. 147–156.

73.

Kampelmacher

, van Noorle Jansen

. Listeriosis in humans and animals in the Netherlands during the past 20 years (1957–1976). In: Symposium on Problems of Listeriosis. Proceedings of the VII International Symposium. Ivanov

(ed.). Varna, Bulgaria, September 23–27, 1977, pp. 264–280.

74.

Kathariou

. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J Food Prot, 2002; 65:1811–1829.

75.

Kathariou

, Graves

, Buchrieser

, Glaser

, Siletzky

, Swaminathan

. Involvement of closely related strains of a new clonal group of Listeria monocytogenes in the 1998–1999 and 2002 multistate outbreaks of foodborne listeriosis in the United States. Foodborne Pathog Dis, 2006; 3:292–302.

76.

Kérouanton

, Marault

, Petit

, Grout

, Dao

, Brisabois

. Evaluation of a multiplex PCR assay as an alternative method for Listeria monocytogenes serotyping. J Microbiol Methods, 2010; 80:134–137.

77.

Kleta

, Hammer

, Dieckmann

, Malorny

, Borowiak

, Halbedel

, Prager

, Trost

, Flieger

, Wilking

, Vygen-Bonnet

, Busch

, Messelhausser

, Horlacher

., Schonberger

, Lohr

, Aichinger

, Luber

, Hensel

, Al Dahouk

. Molecular tracing to find source of protracted invasive listeriosis outbreak, Southern Germany, 2012–2016. Emerg Infect Dis, 2017; 23:1680–1683.

78.

Koch

, Dworak

, Prager

, Becker

, Brockmann

, Wicke

, Wichmann-Schauer

, Hof

, Werber

, Stark

. Large listeriosis outbreak linked to cheese made from pasteurized milk, Germany, 2006–2007. Foodborne Pathog Dis, 2010; 7:1581–1584.

79.

Koch

, Stark

. Significant increase of listeriosis in Germany—epidemiological patterns 2001–2005. Euro Surveill, 2006; 11:85–88.

80.

Lado

, Yousef

. Characteristics of Listeria monocytogenes important to food processors. In: Listeria, Listeriosis and Food Safety, Volume 3, Chaper 6. Ryser

, Marth

(eds.). Boca Raton, FL: CRC Press Taylor and Francis Group, 2007, pp. 157–213.

81.

Laksanalamai

, Joseph

, Silk

, Burall

, Tarr

, Gerner-Smidt

, Datta

. Genomic characterization of Listeria monocytogenes strains involved in a multistate listeriosis outbreak associated with cantaloupe in US. PLoS One, 2012:7:e42448.

82.

Lassen

, Ethelberg

, Björkman

, Jensen

, Sørensen

, Jensen

, Müller

, Nielsen

, Mølbak

. Two Listeria outbreaks caused by smoked fish consumption—using whole-genome sequencing for outbreak investigations. Clin Microbiol Infect, 2016; 22:620–624.

83.

, Perez-Osorio

, Wang

, Eckmann

, Glover

, Allard

, Brown

, Chen

. Whole genome sequencing analyses of Listeria monocytogenes that persisted in a milkshake machine for a year and caused illnesses in Washington State. BMC Microbiol, 2017; 17:1–11.

84.

Linnan

, Mascola

, Lou

, Goulet

, May

, Salminen

, Hird

, Yonekura

, Hayes

, Weaver

, Audurier

, Plikaytis

, Fannin

, Kleks

, Broome

. Epidemic listeriosis associated with Mexican-style cheese. N Engl J Med, 1988; 319:823–828.

85.

Lomonaco

, Nucera

, Filipello

. The evolution and epidemiology of Listeria monocytogenes in Europe and the United States. Infect Genet Evol, 2015; 35:172–183.

86.

Loncarevic

, Danielsson-Tham

, Tham

. Occurrence of Listeria monocytogenes in soft and semi-soft cheeses in retail outlets in Sweden. Int J Food Microbiol, 1995; 26:245–250.

87.

Loncarevic

, Tham

, Danielsson-Tham

. Changes in serogroup distribution among Listeria monocytogenes human isolates in Sweden. In: Program and Abstracts XIII International Symposium on Problems of Listeriosis, Halifax, Nova Scotia, Canada, June 28–July 2, 1988, p. 20.

88.

Lopez-Valladares

, Tham

, Parihar

, Helmersson

, Andersson

, Ivarsson

, Johansson

, Ringberg

, Tjernberg

, Henriques-Normark

, Danielsson-Tham

. Human isolates of Listeria monocytogenes in Sweden during half a century (1958–2010). Epidemiol Infect, 2014; 20:1–10.

89.

Løvdal

. The microbiology of cold smoked salmon. Food Control, 2015; 54:360–373.

90.

Luber

, Crerar

, Dufour

, Farber

, Datta

, Todd

ECD

. Controlling Listeria monocytogenes in ready-to-eat foods: Working towards global scientific consensus and harmonization—recommendations for improved prevention and control. Food Control, 2011; 22:1535–1549.

91.

Lukinmaa

, Miettinen

, Nakari

, Korkeala

, Siitonen

. Listeria monocytogenes isolates from invasive infections: Variation of sero- and genotypes during an 11-year period in Finland. J Clin Microbiol, 2003; 41:1694–1700.

92.

Lyytikäinen

, Nakari

, Lukinmaa

, Kela

, Tran Minh

, Siitonen

. Surveillance of listeriosis in Finland during 1995–2004. Euro Surveill, 2006; 11:82–85.

93.

MacDonald

PDM

, Whitwam

, Boggs

, MacCormack

, Anderson

, Reardon

, Saah

, Graves

, Hunter

, Sobel

. Outbreak of listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican-style cheese. Clin Infect Dis, 2005; 40:677–682.

94.

McIntyre

, Wilcott

, Naus

. Listeriosis outbreaks in British Columbia, Canada, caused by soft ripened cheese contaminated from environmental sources. Biomed Res Int, 2015; 2015:131623.

95.

Magalhães

, Almeida

, Ferreira

, Santos

, Silva

, Mendes

, Pita

, Mariano

, Mancio

, Sousa

. Cheese-related listeriosis outbreak, Portugal, March 2009 to February 2012. Euro Surveill, 2015; 20:14–19.

96.

Magalhães

, Ferreira

, Santos

, Almeida

, Teixeira

, Research

Team

. Genetic and phenotypic characterization of Listeria monocytogenes from human clinical cases that occurred in Portugal between 2008 and 2012. Foodborne Pathog Dis, 2014; 11:907–916.

97.

Makino

, Kawamoto

, Takeshi

, Okada

, Yamasaki

, Yamamoto

, Igimi

. An outbreak of food-borne listeriosis due to cheese in Japan, during 2001. Int J Food Microbiol, 2005; 104:189–196.

98.

Mammina

, Aleo

, Romani

, Pellissier

, Nicoletti

, Pecile

, Nastasi

, Pontello

. Characterization of Listeria monocytogenes isolates from human listeriosis cases in Italy. J Clin Microbiol, 2009:47:2925–2930.

99.

Mammina

, Parisi

, Guaita

, Aleo

, Bonura

, Nastasi

, Pontello

. Enhanced surveillance of invasive listeriosis in the Lombardy region, Italy, in the years 2006–2010 reveals major clones and an increase in serotype 1/2a. BMC Infect Dis, 2013; 13:152.

100.

McLauchlin

. Listeria monocytogenes, recent advances in the taxonomy and epidemiology of listeriosis in humans. J Appl Microbiol, 1987; 63:1–11.

101.

McLauchlin

. The relationship between Listeria and listeriosis. Food Control, 1996a;7:187–193.

102.

McLauchlin

. The role of the Public Health laboratory service in England and Wales in the investigation of human listeriosis during the 1980s and 1990s. Food Control, 1996b;7:235–239.

103.

McLauchlin

, Audurier

, Taylor

. Aspects of the epidemiology of human Listeria monocytogenes infections in Britain 1967–1984; the use of serotyping and phage typing. J Med Microbiol, 1986; 22:367–377.

104.

McLauchlin

, Greenwood

, Pini

. The occurrence of Listeria monocytogenes in cheese from a manufacturer associated with a case of listeriosis. Int J Food Microbiol, 1990; 10:255–262.

105.

McLauchlin

, Hall

, Velani

, Gilbert

. Human listeriosis and pâté. a possible association. Br Med J, 1991; 303:773–775.

106.

McLauchlin

, Mitchell

, Smerdon

, Jewell

. Listeria monocytogenes and listeriosis: A review of hazard characterisation for use in microbiological risk assessment of foods. Int J Food Microbiol, 2004; 92:15–33.

107.

McLauchlin

, Newton

. Human listeriosis in England, Wales and Northern Ireland: A changing pattern of infection. In: Proceedings of the XII International Symposium on Problems of Listeriosis, Perth, Western Australia, October 2–6, 1995, pp. 177–181.

108.

Mead

, Dunne

, Graves

, Wiedmann

, Patrick

, Hunter

, Salehi

, Mostashari

, Craig

, Mshar

, Bannerman

, Sauders

, Hayes

, Dewitt

, Sparling

, Griffin

, Morse

, Slutsker

, Swaminathan

. Nationwide outbreak of listeriosis due to contaminated meat. Nationwide outbreak of listeriosis due to contaminated meat. Epidemiol Infect, 2006; 134:744–751.

109.

Mencikova

. Adnatni listeriosy [Neonatal listeriosis]. Cesk. Epidemiol Mikrobiol Immunol, 1956; 5:225–228.

110.

Miettinen

, Siitonen

, Heiskanen

, Haajanen

, Björkroth

, Korkeala

. Molecular epidemiology of an outbreak of febrile gastroenteritis caused by Listeria monocytogenes in cold-smoked rainbow trout. J Clin Microbiol, 1999; 37:2358–2360.

111.

Nadon

, Woodward

, Young

, Rodgers

, Wiedmann

. Correlations between molecular subtyping and serotyping of Listeria monocytogenes . J Clin Microbiol, 2001; 39:2704–2707.

112.

Nakama

, Terao

, Kokubo

, Itoh

, Maruyama

, Kaneuchi

, McLauchlin

. A comparison of Listeria monocytogenes serovar 4b isolates of clinical and food origin in Japan by pulsed-field gel electrophoresis. Int J Food Microbiol, 1998; 42:201–206.

113.

Nho

, Abdelhamed

, Reddy

, Karsi

, Lawrence

. Identification of high-risk Listeria monocytogenes serotypes in lineage I (serotype 1/2a, 1/2c, 3a and 3c) using multiplex PCR. J Appl Microbiol, 2015; 119:845–852.

114.

Okpo

, Leith

, Smith-Palmer

, Bell

, Parks

, Browning

, Byers

, Corrigan

, Webster

, Karcher

, Murray

, Storey

. An outbreak of an unusual strain of Listeria monocytogenes infection in North-East Scotland. J Infect Public Health, 2015; 8:612–618.

115.

Olsen

, Patrick

, Hunter

, Reddy

, Kornstein

, MacKenzie

, Lane

, Bidol

, Stoltman

, Frye

, Lee

, Hurd

, Jones

, LaPorte

, Dewitt

, Graves

, Wiedmann

, Schoonmaker-Bopp

, Huang

, Vincent

, Bugenhagen

, Corby

, Carloni

, Holcomb

, Woron

, Zansky

, Dowdle

, Smith

, Ahrabi-Fard

, Ong

, Tucker

, Hynes

, Mead

. Multistate outbreak of Listeria monocytogenes infection linked to delicatessen turkey meat. Clin Infect Dis, 2005; 40:962–967.

116.

Orsi

, den Backer

, Wiedmann

. Listeria monocytogenes lineages: Genomics, evolution, ecology and phenotypic characteristics. Int J Med Microbiol, 2011; 301:79–96.

117.

Pagotto

, Ng

, Clark

, Farber

. Canadian listeriosis reference service. Foodborne Pathog Dis, 2006; 3:132–137.

118.

Pak

, Spahr

, Jemmi

, Salman

. Risk factors for L. monocytogenes contamination of dairy products in Switzerland, 1990–1999. Prev Vet Med, 2002; 53:55–65.

119.

Paudyal

, Anihouvi

, Hounhouigan

, Matsheka

, Sekwati-Monang

, Amoa-Awua

, Atter

, Ackah

, Mbugua

, Asagbra

, Abdelgadir

, Nakavuma

, Jakobsen

, Fang

. Prevalence of foodborne pathogens in food from selected African countries—a meta-analysis. Int J Food Microbiol, 2017; 249:35–43.

120.

Pichler

, Much

, Kasper

, Fretz

, Auer

, Kathan

, Mann

, Huhulescu

, Ruppitsch

, Pietzka

, Silberbauer

, Neumann

, Gschiel

, De Martin

, Schuetz

, Gindl

, Neugschwandtner

, Allerberger

. An outbreak of febrile gastroenteritis associated with jellied pork contaminated with Listeria monocytogenes . Wiener Klin Wochenschr, 2009; 121:149–156.

121.

Pontello

, Guaita

, Sala

, Cipolla

, Gattuso

, Sonnessa

, Gianfranceschi

. Listeria monocytogenes serotypes in human infections (Italy, 2000–2010). Annali dell'Istituto Superiore di Sanità, 2012; 48:146–150.

122.

Pouillot

, Goulet

, Delignette-Muller

, Mahé

, Cornu

. Quantitative risk assessment of Listeria monocytogenes in French cold-smoked salmon: II. Risk Anal, 2009; 29:806–819.

123.

Radostits

, Blood

, Gay

, eds. Diseases caused by Listeria spp. In: Veterinary Medicine, 8 ^th ed. London, England: Baillière and Tindall, 1994, pp. 660–666.

124.

Raheem

. Outbreaks of listeriosis associated with deli meats and cheese: An overview. AIMS Microbiol, 2016; 2:230–250.

125.

Rasmussen

, Skouboe

, Dons

, Rossen

, Olsen

. Listeria monocytogenes exists in at least three evolutionary lines: Evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiology, 1995; 141:2053–2062.

126.

Rocourt

, Jacquet

, Reilly

. Epidemiology of human listeriosis and seafoods. Int J Food Microbiol, 2000; 62:197–209.

127.

Rosef

, Klæboe

, Paulauskas

, Ambrasiene

. Diversity of Listeria monocytogenes isolated from humans, food, and environmental sources in Norway. Veterinarija ir Zootechnika, 2012; 59:71–79.

128.

Samuelsson

, Rothgardt

, Carvajal

, Frederiksen

. Human listeriosis in Denmark 1981–1987 Including an outbreak November 1985–March 1987. J Infect, 1990; 20:251–259.

129.

Sanaa

, Coroller

, Cerf

. Risk assessment of listeriosis linked to the consumption of two soft cheeses made from raw milk: Camembert of Normandy and Brie of Meaux. Risk Anal, 2004; 24:389–399.

130.

Schlech

, Lavigne

, Bortolussi

, Allen

, Haldane

, Wort

, Hightower

, Johnson

, King

, Nicholls

, Broome

. Epidemic listeriosis: Evidence for transmission by food. N Engl J Med, 1983; 308:203–206.

131.

Schwartz

, Hexter

, Broome

, Hightower

, Hirschhorn

, Porter

, Hayes

, Bibb

, Lorber

, Faris

. Investigation of an outbreak of listeriosis—new hypotheses for the etiology of epidemic Listeria monocytogenes infections. J Infect Dis, 1989; 159:680–685.

132.

Seeliger

. Listeriosis. [Contributions to hygiene and epidemiology] Beiträge zur Hygiene und Epidemiologie, Heft 8 . Leipzig, Germany: Johann Ambrosius Barth, 1955, pp. 154.

133.

Seeliger

HPR

. Listeriosis. Basel, Switzerland: S. Karger AG, 1961, pp. 308.

134.

Seeliger

HPR

, Höhne

. Chapter II Serotyping of Listeria monocytogenes and related species. Methods Microbiol, 1979; 13:31–49.

135.

Seeliger

HPR

, Jones

. Genus Listeria. In: Bergey's Manual of Systematic Bacteriology, Volume 2. Sneath

PHA

, Mair

, Sharpe

, Holt

(eds.). Baltimore, MD: The Williams and Wilkins Co., 1986, pp. 1235–1245.

136.

Sepp

, Roy

. Listeria monocytogenes infections in metropolitan Toronto. A clinicopathological study. Can Med Assoc J, 1963; 88:549–561.

137.

Shetty

, McLauchlin

, Grant

, O'Brien

, Howard

, Davies

. Outbreak of Listeria monocytogenes in an oncology unit associated with sandwiches consumed in hospital. J Hosp Infect, 2009; 72:332–336.

138.

Sipka

, Zakula

, Kovincic

, Staiiner

. Secretion of Listeria monocytogenes in cow's milk and its survival in white brined cheese. In: Proceedings of the XIX International Dairy Congress. New Delhi, India: 1974, 1E, p. 157.

139.

Smith

, Larsson

, Lisby

, Muller

, Madsen

, Engberg

, Bangsborg

, Ethelberg

, Kemp

. Outbreak of listeriosis caused by infected beef meat from a meals-on-wheels delivery in Denmark 2009. Clin Microbiol Infect, 2011; 17:50–52.

140.

Stephan

, Althaus

, Kiefer

, Lehner

, Hatz

, Schmutz

, Jost

, Gerber

, Baumgartner

, Hachler

, Mausezahl-Feuz

. Foodborne transmission of Listeria monocytogenes via ready-to-eat salad: A nationwide outbreak in Switzerland, 2013–2014. Food Control, 2015; 57:14–17.

141.

Sutherland

, Miles

, Laboyrie

. Listeria monocytogenes. In: Foodborne Microorganisms of Public Health Significance, Chapter 13, 6 ^th ed. Hocking

(ed.). Sydney, Australia: Australian Institute of Food Science and Technology (NSW Branch), 2003, pp. 381–443.

142.

Swaminathan

, Gerner-Smidt

. The epidemiology of human listeriosis. Microb Infect, 2007; 9:1236–1243.

143.

Todd

ECD

, Notermans

. Surveillance of listeriosis and its causative pathogen, Listeria monocytogenes . Food Control, 2011; 22:1484–1490.

144.

Tompkin

. Control of Listeria monocytogenes in the food-processing environment. J Food Prot, 2002; 65:709–725.

145.

Tran

THC

, Campbell

, Schultsz

, Nguyen

, Diep

. Baker S, Nguyen TC. Farrar JJ, van Doorn HR. Three adult cases of Listeria monocytogenes meningitis in Vietnam. PLoS Med, 2010; 7:e1000306.

146.

Vázquez-Boland

, Kuhn

, Berche

, Chakraborty

, Domínguez-Bernal

, Goebel

, González-Zorn

, Wehland

, Kreft

. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev, 2001; 14:584–640.

147.

Vela

, Fernandez-Garayzabal

, Vasquez

, Latre

, Blanco

, Moreno

, de la Fuente

, Marco

, Franco

, Cepeda

, Rodriguez Moure

, Suarez

. Dominguez L. Molecular typing by pulsed-field gel electrophoresis of Spanish animal and human Listeria monocytogenes isolates. Appl Environ Microbiol, 2001; 67:5840–5843.

148.

Wiedmann

. Molecular subtyping methods for Listeria monocytogenes . J AOAC Int, 2002; 85:524–531.

149.

Wiedmann

, Bruce

, Keating

, Johnson

, McDonough

, Batt

. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun, 1997; 65:2707–2716.

150.

Yde

, Naranjo

, Mattheus

, Stragier

, Pochet

, Beulens

, De Schrijver

, Van den Branden

, Laisnez

, Flipse

, Leclercq

, Lecuit

, Dierick

, Bertrand

. Usefulness of the European Epidemic Intelligence Information System in the management of an outbreak of listeriosis, Belgium, 2011. Euro Surveill, 2012; 17:2–6.