The overgrowth of Listeria monocytogenes by other Listeria spp. in food samples undergoing enrichment cultivation has a nutritional basis

Besse, Nathalie Gnanou; Barre, Léna; Buhariwalla, Colin F.; Vignaud, Marie-Léone; Khamissi, Elissa; Decourseulles, Emilie; Nirsimloo, Marjorie; Chelly, Minyar; Kalmokoff, Martin

doi:10.1016/j.ijfoodmicro.2009.10.025

Cited by 66 publications

(44 citation statements)

References 19 publications

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“…are often co-isolated from L. monocytogenes-positive food samples (Angelidis and Koutsoumanis, 2006;Greenwood et al, 1991;Jamali et al, 2013). In addition, the presence of L. innocua in L. monocytogenes-contaminated foods may negatively affect the chances of detecting L. monocytogenes (Gnanou-Besse et al, 2005;Gnanou-Besse et al, 2010;Zitz et al, 2011). Hence, the presence of non-pathogenic Listeria spp.…”

Section: Introductionmentioning

confidence: 99%

Identification of non-Listeria spp. bacterial isolates yielding a β-d-glucosidase-positive phenotype on Agar Listeria according to Ottaviani and Agosti (ALOA)

Angelidis

Kalamaki

Georgiadou

2015

International Journal of Food Microbiology

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Section: Introductionmentioning

confidence: 99%

Identification of non-Listeria spp. bacterial isolates yielding a β-d-glucosidase-positive phenotype on Agar Listeria according to Ottaviani and Agosti (ALOA)

Angelidis

Kalamaki

Georgiadou

2015

International Journal of Food Microbiology

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“…The interference of background food microflora (9,10) or other Listeria spp. (particularly L. innocua) may mask the presence and diminish the detectability of L. monocytogenes (11)(12)(13)(14)(15)(16)(17). Recent studies have addressed the issue of L. monocytogenes strain competition as a factor related to enrichment bias (18,19).…”

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confidence: 99%

Listeria monocytogenes Strains Underrepresented during Selective Enrichment with an ISO Method Might Dominate during Passage through Simulated Gastric Fluid and In Vitro Infection of Caco-2 Cells

Zilelidou

Karmiri

Ζουμποπούλου

et al. 2016

Appl Environ Microbiol

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Various Listeria monocytogenes strains may contaminate a single food product, potentially resulting in simultaneous exposure of consumers to multiple strains. However, due to bias in strain recovery, L. monocytogenes strains isolated from foods by selective enrichment (SE) might not always represent those that can better survive the immune system of a patient. We investigated the effect of cocultivation in tryptic soy broth with 0.6% yeast extract (TSB-Y) at 10°C for 8 days on (i) the detection of L. monocytogenes strains during SE with the ISO 11290-1:1996/Amd 1:2004 protocol and (ii) the in vitro virulence of strains toward the Caco-2 human colon epithelial cancer cell line following exposure to simulated gastric fluid (SGF; pH 2.0)-HCl (37°C). We determined whether the strains which were favored by SE would be effective competitors under the conditions of challenges related to gastrointestinal passage of the pathogen. Interstrain competition of L. monocytogenes in TSB-Y determined the relative population of each strain at the beginning of SE. This in turn impacted the outcome of SE (i.e., favoring survival of competitors with better fitness) and the levels exposed subsequently to SGF. However, strong growth competitors could be outcompeted after SGF exposure and infection of Caco-2 cells by strains outgrown in TSB-Y and underdetected (or even missed) during enrichment. Our data demonstrate a preferential selection of certain L. monocytogenes strains during enrichments, often not reflecting a selective advantage of strains during infection. These findings highlight a noteworthy scenario associated with the difficulty of matching the source of infection (food) with the L. monocytogenes isolate appearing to be the causative agent during listeriosis outbreak investigations. IMPORTANCEThis report is relevant to understanding the processes involved in selection and prevalence of certain L. monocytogenes strains in different environments (i.e., foods or sites of humans exposed to the pathogen). It highlights the occurrence of multiple strains in the same food as an important aspect contributing to mismatches between clinical isolates and infection sources during listeriosis outbreak investigations. Selective enrichment (SE) for detection of foodborne pathogens has been a fundamental tool in the food industry, critical for hygiene control and safety monitoring (1) while providing crucial information during trace-back investigations of foodborne outbreaks. However, selective culture-based enrichment procedures are associated with inherent bias since the use of selective agents and the presence of competing background microorganisms in food samples sometimes obstruct the isolation of a target pathogen and lead to false-negative results (2, 3).Listeria monocytogenes stands out among the pathogens of major concern for food safety. This Gram-positive bacterium causes the rare but life-threatening disease listeriosis and manifests the interplay between saprophytic lifestyle and virulence (4, 5). Its ubiquity allows...

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“…This may not correspond to the reality. It has been proposed that the advantages of L. innocua over L. monocytogenes could be due to physiological characteristics, such as growth rates (6); to nutritional competition (26); or to the production of bacterial-growth-inhibiting factors (9), the majority of inhibitors are phages or phage tails. All Listeria-specific phages found to date are members of the Caudovirales, featuring the long, noncontractile tails of the family Siphoviridae or the complex contractile-tail machines of the family Myoviridae (27).…”

Section: Discussionmentioning

confidence: 99%

“…L. monocytogenes serogroup 4 strains produce monocin type B, which is active only against L. monocytogenes serotypes 4a and 4c and L. ivanovii, whereas L. monocytogenes serogroup 1 strains produce monocin types C, D, and E, which are active against L. monocytogenes serotype 4b strains, in addition to serotypes 4a and 4c and L. ivanovii. This type of competition, along with other factors, such as nutrition (26), could explain the predominance of L. monocytogenes serogroup 1 found in food and in environmental sources and the involvement of phages or phage tails in overgrowth of L. monocytogenes by other Listeria species during enrichment steps of the detection assays.…”

Section: Discussionmentioning

confidence: 99%

Listeria Phage and Phage Tail Induction Triggered by Components of Bacterial Growth Media (Phosphate, LiCl, Nalidixic Acid, and Acriflavine)

Lemaı̂tre

Duroux

Pimpie

et al. 2015

Appl Environ Microbiol

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The detection of Listeria monocytogenes from food is currently carried out using a double enrichment. For the ISO methodology, this double enrichment is performed using half-Fraser and Fraser broths, in which the overgrowth of L. innocua can occur in samples where both species are present. In this study, we analyzed the induction of phages and phage tails of Listeria spp. in these media and in two brain heart infusion (BHI) broths (BHIM [bioMérieux] and BHIK [Biokar]) to identify putative effectors. It appears that Na 2 HPO 4 at concentrations ranging from 1 to 40 g/liter with an initial pH of 7.5 can induce phage or phage tail production of Listeria spp., especially with 10 g/liter of Na 2 HPO 4 and a pH of 7.5, conditions present in half-Fraser and Fraser broths. Exposure to LiCl in BHIM (18 to 21 g/liter) can also induce phage and phage tail release, but in half-Fraser and Fraser broths, the concentration of LiCl is much lower (3 g/liter). Low phage titers were induced by acriflavine and/or nalidixic acid. We also show that the production of phages and phage tails can occur in half-Fraser and Fraser broths. This study points out that induction of phages and phage tails could be triggered by compounds present in enrichment media. This could lead to a false-negative result for the detection of L. monocytogenes in food products.T he widespread prevalence of Listeria monocytogenes in food products, the severity of illness caused, and the number of reported outbreaks require fast and reliable detection of the pathogen (1). Moreover, the detection method has to be sensitive enough to detect L. monocytogenes at levels as low as 1 cell per gram of food material. This usually involves selective enrichment procedures due to both the low density of these microorganisms and the high levels of background microflora that are normally simultaneously present. For this detection, the ISO 11290-1 reference method is recommended; the first enrichment is performed in half-Fraser broth and the second in Fraser broth (2). Several studies showed that L. innocua and L. monocytogenes were found together in food, with L. innocua being more frequently isolated than L. monocytogenes (3,4). This could result from the evolution of the ratio between these species during the enrichment process in an way that was advantageous for L. innocua. Competition between L. monocytogenes strains of different serotypes is also possible and has been demonstrated between serotypes 1 and 4 (5). These competitions could be due either to nutritional factors (components of the growth medium can differentially favor bacterial multiplication) or to the production of compounds inhibiting L. monocytogenes growth (3, 6-8). Kalmokoff et al. (9) showed that, among 300 Listeria strains tested, 71% produced phages or phage tails (68% of 50 L. innocua strains). Thus, during the enrichment steps necessary for the multiplication of the Listeria strains, the growth of nonpathogenic species could cause falsenegative detection of low levels of L. monocytogenes (10). Until...

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The overgrowth of Listeria monocytogenes by other Listeria spp. in food samples undergoing enrichment cultivation has a nutritional basis

Cited by 66 publications

References 19 publications

Identification of non-Listeria spp. bacterial isolates yielding a β-d-glucosidase-positive phenotype on Agar Listeria according to Ottaviani and Agosti (ALOA)

Identification of non-Listeria spp. bacterial isolates yielding a β-d-glucosidase-positive phenotype on Agar Listeria according to Ottaviani and Agosti (ALOA)

Listeria monocytogenes Strains Underrepresented during Selective Enrichment with an ISO Method Might Dominate during Passage through Simulated Gastric Fluid and In Vitro Infection of Caco-2 Cells

Listeria Phage and Phage Tail Induction Triggered by Components of Bacterial Growth Media (Phosphate, LiCl, Nalidixic Acid, and Acriflavine)

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