Matthew J. Stasiewicz
Cornell University
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Journal of Food Protection | 2014
V. Ferreira; Martin Wiedmann; Paula Teixeira; Matthew J. Stasiewicz
Over the last 10 to 15 years, increasing evidence suggests that persistence of Listeria monocytogenes in food processing plants for years or even decades is an important factor in the transmission of this foodborne pathogen and the root cause of a number of human listeriosis outbreaks. L. monocytogenes persistence in other food-associated environments (e.g., farms and retail establishments) may also contribute to food contamination and transmission of the pathogen to humans. Although L. monocytogenes persistence is typically identified through isolation of a specific molecular subtype from samples collected in a given environment over time, formal (statistical) criteria for identification of persistence are undefined. Environmental factors (e.g., facilities and equipment that are difficult to clean) have been identified as key contributors to persistence; however, the mechanisms are less well understood. Although some researchers have reported that persistent strains possess specific characteristics that may facilitate persistence (e.g., biofilm formation and better adaptation to stress conditions), other researchers have not found significant differences between persistent and nonpersistent strains in the phenotypic characteristics that might facilitate persistence. This review includes a discussion of our current knowledge concerning some key issues associated with the persistence of L. monocytogenes, with special focus on (i) persistence in food processing plants and other food-associated environments, (ii) persistence in the general environment, (iii) phenotypic and genetic characteristics of persistent strains, (iv) niches, and (v) public health and economic implications of persistence. Although the available data clearly indicate that L. monocytogenes persistence at various stages of the food chain contributes to contamination of finished products, continued efforts to quantitatively integrate data on L. monocytogenes persistence (e.g., meta-analysis or quantitative microbial risk assessment) will be needed to advance our understanding of persistence of this pathogen and its economic and public health impacts.
International Journal of Systematic and Evolutionary Microbiology | 2014
Henk C. den Bakker; Steven Warchocki; Emily M. Wright; Adam F. Allred; Christina Ahlstrom; Clyde S. Manuel; Matthew J. Stasiewicz; Angela Burrell; Sherry Roof; Laura K. Strawn; Esther D. Fortes; Kendra K. Nightingale; Daniel Kephart; Martin Wiedmann
Sampling of agricultural and natural environments in two US states (Colorado and Florida) yielded 18 Listeria-like isolates that could not be assigned to previously described species using traditional methods. Using whole-genome sequencing and traditional phenotypic methods, we identified five novel species, each with a genome-wide average BLAST nucleotide identity (ANIb) of less than 85% to currently described species. Phylogenetic analysis based on 16S rRNA gene sequences and amino acid sequences of 31 conserved loci showed the existence of four well-supported clades within the genus Listeria; (i) a clade representing Listeria monocytogenes, L. marthii, L. innocua, L. welshimeri, L. seeligeri and L. ivanovii, which we refer to as Listeria sensu stricto, (ii) a clade consisting of Listeria fleischmannii and two newly described species, Listeria aquatica sp. nov. (type strain FSL S10-1188(T) = DSM 26686(T) = LMG 28120(T) = BEI NR-42633(T)) and Listeria floridensis sp. nov. (type strain FSL S10-1187(T) = DSM 26687(T) = LMG 28121(T) = BEI NR-42632(T)), (iii) a clade consisting of Listeria rocourtiae, L. weihenstephanensis and three novel species, Listeria cornellensis sp. nov. (type strain TTU A1-0210(T) = FSL F6-0969(T) = DSM 26689(T) = LMG 28123(T) = BEI NR-42630(T)), Listeria grandensis sp. nov. (type strain TTU A1-0212(T) = FSL F6-0971(T) = DSM 26688(T) = LMG 28122(T) = BEI NR-42631(T)) and Listeria riparia sp. nov. (type strain FSL S10-1204(T) = DSM 26685(T) = LMG 28119(T) = BEI NR- 42634(T)) and (iv) a clade containing Listeria grayi. Genomic and phenotypic data suggest that the novel species are non-pathogenic.
Applied and Environmental Microbiology | 2011
V. Ferreira; Joana Barbosa; Matthew J. Stasiewicz; Kitiya Vongkamjan; A. Moreno Switt; Tim Hogg; Paul Gibbs; Paula Teixeira; Martin Wiedmann
ABSTRACT The persistence of Listeria monocytogenes in food-associated environments represents a key factor in transmission of this pathogen. To identify persistent and transient strains associated with production of fermented meat sausages in northern Portugal, 1,723 L. monocytogenes isolates from raw material and finished products from 11 processors were initially characterized by random amplification of polymorphic DNA (RAPD), PCR-based molecular serotyping, and epidemic clone characterization, as well as cadmium, arsenic, and tetracycline resistance typing. Pulsed-field gel electrophoresis (PFGE) typing of 240 representative isolates provided evidence for persistence of L. monocytogenes for periods of time ranging from 10 to 32 months for all seven processors for which isolates from different production dates were available. Among 50 L. monocytogenes isolates that included one representative for each PFGE pattern obtained from a given sample, 12 isolates showed reduced invasion efficiency in Caco-2 cells, including 8 isolates with premature stop codons in inlA. Among 41 isolates representing sporadic and persistent PFGE types, 22 isolates represented lysogens. Neither strains with reduced invasion nor lysogens were overrepresented among persistent isolates. While the susceptibility of isolates to lysogenic phages also did not correlate with persistence, it appeared to be associated with molecular serotype. Our data show the following. (i) RAPD may not be suitable for analysis of large sets of L. monocytogenes isolates. (ii) While a large diversity of L. monocytogenes subtypes is found in Portuguese fermented meat sausages, persistence of L. monocytogenes in this food chain is common. (iii) Persistent L. monocytogenes strains are diverse and do not appear to be characterized by unique genetic or phenotypic characteristics.
Applied and Environmental Microbiology | 2015
Matthew J. Stasiewicz; Haley F. Oliver; Martin Wiedmann; Henk C. den Bakker
ABSTRACT While the food-borne pathogen Listeria monocytogenes can persist in food associated environments, there are no whole-genome sequence (WGS) based methods to differentiate persistent from sporadic strains. Whole-genome sequencing of 188 isolates from a longitudinal study of L. monocytogenes in retail delis was used to (i) apply single-nucleotide polymorphism (SNP)-based phylogenetics for subtyping of L. monocytogenes, (ii) use SNP counts to differentiate persistent from repeatedly reintroduced strains, and (iii) identify genetic determinants of L. monocytogenes persistence. WGS analysis revealed three prophage regions that explained differences between three pairs of phylogenetically similar populations with pulsed-field gel electrophoresis types that differed by ≤3 bands. WGS-SNP-based phylogenetics found that putatively persistent L. monocytogenes represent SNP patterns (i) unique to a single retail deli, supporting persistence within the deli (11 clades), (ii) unique to a single state, supporting clonal spread within a state (7 clades), or (iii) spanning multiple states (5 clades). Isolates that formed one of 11 deli-specific clades differed by a median of 10 SNPs or fewer. Isolates from 12 putative persistence events had significantly fewer SNPs (median, 2 to 22 SNPs) than between isolates of the same subtype from other delis (median up to 77 SNPs), supporting persistence of the strain. In 13 events, nearly indistinguishable isolates (0 to 1 SNP) were found across multiple delis. No individual genes were enriched among persistent isolates compared to sporadic isolates. Our data show that WGS analysis improves food-borne pathogen subtyping and identification of persistent bacterial pathogens in food associated environments.
Applied and Environmental Microbiology | 2011
Matthew J. Stasiewicz; Martin Wiedmann; Teresa M. Bergholz
ABSTRACT The organic acids lactate and diacetate are commonly used in combination in ready-to-eat foods because they show synergistic ability to inhibit the growth of Listeria monocytogenes. Full-genome microarrays were used to investigate the synergistic transcriptomic responses of two L. monocytogenes strains, H7858 (serotype 4b) and F6854 (serotype 1/2a), to these two organic acids under conditions representing osmotic and cold stress encountered in foods. Strains were exposed to brain heart infusion (BHI) broth at 7°C with 4.65% water-phase (w.p.) NaCl at pH 6.1 with (i) 2% w.p. potassium lactate, (ii) 0.14% w.p. sodium diacetate, (iii) the combination of both at the same levels, or (iv) no organic acids as a control. RNA was extracted 8 h after exposure, during lag phase, to capture gene transcription changes during adaptation to the organic acid stress. Significant differential transcription of 1,041 genes in H7858 and 640 genes in F6854 was observed in at least one pair of the 4 different treatments. The effects of combined treatment with lactate and diacetate included (i) synergistic transcription differences for 474 and 209 genes in H7858 and F6854, respectively, (ii) differential transcription of genes encoding cation transporters and ABC transporters of metals, and (iii) altered metabolism, including induction of a nutrient-limiting stress response, reduction of menaquinone biosynthesis, and a shift from fermentative production of acetate and lactate to energetically less favorable, neutral acetoin. These data suggest that additional treatments that interfere with cellular energy generation processes could more efficiently inhibit the growth of L. monocytogenes.
Journal of Food Protection | 2014
Courtenay Simmons; Matthew J. Stasiewicz; Emily M. Wright; Steven Warchocki; Sherry Roof; Janell Kause; Nathan Bauer; Salam A. Ibrahim; Martin Wiedmann; Haley F. Oliver
Postprocessing contamination in processing plants has historically been a significant source of Listeria monocytogenes in ready-to-eat delicatessen meats, and therefore a major cause of human listeriosis cases and outbreaks. Recent risk assessments suggest that a majority of human listeriosis cases linked to consumption of contaminated deli meats may be due to L. monocytogenes contamination that occurs at the retail level. To better understand the ecology and transmission of Listeria spp. in retail delicatessens, food and nonfood contact surfaces were tested for L. monocytogenes and other Listeria spp. in a longitudinal study conducted in 30 retail delis in three U.S. states. In phase I of the study, seven sponge samples were collected monthly for 3 months in 15 delis (5 delis per state) prior to start of daily operation; in phase II, 28 food contact and nonfood contact sites were sampled in each of 30 delis during daily operation for 6 months. Among the 314 samples collected during phase I, 6.8% were positive for L. monocytogenes. Among 4,503 samples collected during phase II, 9.5% were positive for L. monocytogenes; 9 of 30 delis showed low L. monocytogenes prevalence (<1%) for all surfaces. A total of 245 Listeria spp. isolates, including 184 Listeria innocua, 48 Listeria seeligeri, and 13 Listeria welshimeri were characterized. Pulsed-field gel electrophoresis (PFGE) was used to characterize 446 L. monocytogenes isolates. PFGE showed that for 12 of 30 delis, one or more PFGE types were isolated on at least three separate occasions, providing evidence for persistence of a given L. monocytogenes subtype in the delis. For some delis, PFGE patterns for isolates from nonfood contact surfaces were distinct from patterns for occasional food contact surface isolates, suggesting limited cross-contamination between these sites in some delis. This study provides longitudinal data on L. monocytogenes contamination patterns in retail delis, which should facilitate further development of control strategies in retail delis.
Journal of Food Protection | 2008
Matthew J. Stasiewicz; Bradley P. Marks; Alicia Orta-Ramirez; D. M. Smith
Traditional models for predicting the thermal inactivation rate of bacteria are state dependent, considering only the current state of the product. In this study, the potential for previous sublethal thermal history to increase the thermotolerance of Salmonella in ground turkey was determined, a path-dependent model for thermal inactivation was developed, and the path-dependent predictions were tested against independent data. Weibull-Arrhenius parameters for Salmonella inactivation in ground turkey thigh were determined via isothermal tests at 55, 58, 61, and 63 degrees C. Two sets of nonisothermal heating tests also were conducted. The first included five linear heating rates (0.4, 0.9, 1.7, 3.5, and 7.0 K/min) and three holding temperatures (55, 58, and 61 degrees C); the second also included sublethal holding periods at 40, 45, and 50 degrees C. When the standard Weibull-Arrhenius model was applied to the nonisothermal validation data sets, the root mean squared error of prediction was 2.5 log CFU/g, with fail-dangerous residuals as large as 4.7 log CFU/g when applied to the complete nonisothermal data set. However, by using a modified path-dependent model for inactivation, the prediction errors for independent data were reduced by 56%. Under actual thermal processing conditions, use of the path-dependant model would reduce error in thermal lethality predictions for slowly cooked products.
Journal of Food Protection | 2013
Thomas J. V. Malley; Matthew J. Stasiewicz; Yrjö T. Gröhn; Sherry Roof; Steven Warchocki; Kendra K. Nightingale; Martin Wiedmann
Listeria monocytogenes persistence in food processing plants is a key source of postprocessing contamination of ready-to-eat foods. Thus, identification and elimination of sites where L. monocytogenes persists (niches) is critical. Two smoked fish processing plants were used as models to develop and implement environmental sampling plans (i) to identify persistent L. monocytogenes subtypes (EcoRI ribotypes) using two statistical approaches and (ii) to identify and eliminate likely L. monocytogenes niches. The first statistic, a binomial test based on ribotype frequencies, was used to evaluate L. monocytogenes ribotype recurrences relative to reference distributions extracted from a public database; the second statistic, a binomial test based on previous positives, was used to measure ribotype occurrences as a risk factor for subsequent isolation of the same ribotype. Both statistics revealed persistent ribotypes in both plants based on data from the initial 4 months of sampling. The statistic based on ribotype frequencies revealed persistence of particular ribotypes at specific sampling sites. Two adaptive sampling strategies guided plant interventions during the study: sampling multiple times before and during processing and vector swabbing (i.e., sampling of additional sites in different directions [vectors] relative to a given site). Among sites sampled for 12 months, a Poisson model regression revealed borderline significant monthly decreases in L. monocytogenes isolates at both plants (P = 0.026 and 0.076). Our data indicate elimination of an L. monocytogenes niche on a food contact surface; niches on nonfood contact surfaces were not eliminated. Although our data illustrate the challenge of identifying and eliminating L. monocytogenes niches, particularly at nonfood contact sites in small and medium plants, the methods for identification of persistence we describe here should broadly facilitate science-based identification of microbial persistence.
International Journal of Food Microbiology | 2013
Silin Tang; Matthew J. Stasiewicz; Martin Wiedmann; Kathryn J. Boor; Teresa M. Bergholz
Listeria monocytogenes is of particular concern in cold-smoked fish products as it can survive curing and cold-smoking, and can subsequently grow from low numbers to potentially hazardous levels during refrigerated storage. The purpose of this study was to (i) quantify the effects of organic acids, nisin, and their combinations on controlling L. monocytogenes growth on cold-smoked salmon at refrigeration temperatures, (ii) identify synergistic interactions of binary combinations of these antimicrobials, and (iii) determine if results from laboratory growth media can predict antimicrobial efficacy on cold-smoked salmon. Strains representing the genetic diversity of L. monocytogenes lineages I and II were grown in brain heart infusion (BHI) broth as well as on the surface of commercially produced wet-cured, cold-smoked salmon slices at 7°C. BHI broth and cold-smoked salmon were supplemented with sodium diacetate (SDA, 0.14% water phase (w.p.)), potassium lactate (PL, 2% w.p.), nisin (NI, 50ppm), and binary combinations of inhibitors at the same levels. Cell densities of L. monocytogenes were measured over time and used to calculate growth parameters, including initial cell density (N0), lag phase (λ), maximum growth rate (μmax), and maximum cell density (Nmax) for each antimicrobial treatment. N0 was significantly lowered by addition of NI with a similar average reduction on salmon (2.02±0.99 log(CFU/g)) and in BHI (1.51±0.83 log(CFU/ml)). Among all antimicrobial treatments, the combination of PL and SDA led to the greatest increase in λ both on salmon (7.1±3.6days) and in BHI (9.7±3.8days) when compared to the controls. The combination of PL and SDA had synergistic effects on increasing λ and lowering Nmax both in BHI and on salmon. Among all the treatments tested, the combination of NI and PL led to the greatest reductions in Nmax on salmon. We observed positive correlations between the growth parameters obtained from BHI broth and cold-smoked salmon, indicating that growth of L. monocytogenes in broth, to some extent, qualitatively reflected characteristics of growth on cold-smoked salmon under antimicrobial stresses. Results from BHI could quantitatively predict the variability of growth parameters obtained from salmon for lineage II strains, but not for lineage I strains. Although results from laboratory growth medium may not provide exact predictions of antimicrobial efficacy on cold-smoked salmon, they could be used to rapidly identify effective combinations for further examination on cold-smoked salmon.
Journal of Food Protection | 2010
Matthew J. Stasiewicz; Martin Wiedmann; Teresa M. Bergholz
Combinations of organic acids are often used in ready-to-eat foods to control the growth of Listeria monocytogenes during refrigerated storage. The purpose of this study was to quantitatively assess synergy between two organic acid growth inhibitors under conditions similar to those present in cold-smoked salmon, and to assess the effect of evolutionary lineage on response to those growth inhibitors. Thirteen strains of L. monocytogenes, representing lineages I and II, were grown at 7 degrees C in broth at pH 6.1 and 4.65% water-phase NaCl, which was supplemented with 2% potassium lactate, 0.14% sodium diacetate, or the combination of both at the same levels. Our data suggest that lineages adapt similarly to these inhibitors, as the only significant growth parameter difference between lineages was a minor effect (+/- 0.16 day, P = 0.0499) on lag phase (lambda). For all strains, lactate significantly extended lambda, from 2.6 +/- 0.4 to 3.8 +/- 0.5 days (P < 0.001), and lowered the maximum growth rate (mu(max)) from 0.54 +/- 0.06 to 0.49 +/- 0.04 log(CFU/ml)/day (P < 0.001), compared with the control. Diacetate was ineffective alone, but in combination with lactate, synergistically increased lambda to 6.6 +/- 1.6 days (P < 0.001) and decreased mu(max) to 0.34 +/- 0.05 log(CFU/ml)/day (P < 0.001). Monte Carlo simulations provided further evidence for synergy between diacetate and lactate by predicting signficantly slower growth to nominal endpoints for the combination of inhibitors. This study shows potassium lactate and sodium diacetate have significant synergistic effects on both lambda and mu(max) of L. monocytogenes at refrigeration temperature in broth, and justifies combining these inhibitors, at effective levels, in food product formulations.