Persistent and transient Listeria monocytogenes strains from retail deli environments vary in their ability to adhere and form biofilms and rarely have inlA premature stop codons

Foodborne Pathogens and Disease

Volumn 12, Issue 2, 2015, Pages 151-158

  Wang, Jingjin ^a   Ray, Andrea J ^a   Hammons, Susan R ^a   Oliver, Haley F ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BIOFILM; CONTROLLED STUDY; ENVIRONMENT; GENE; INLA GENE; LISTERIA MONOCYTOGENES; LISTERIOSIS; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; RISK ASSESSMENT; STOP CODON; UNITED STATES; WILD TYPE; ANTIBIOTIC RESISTANCE; CATERING SERVICE; DRUG EFFECTS; ECONOMICS; FOODBORNE DISEASES; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; KITCHEN; MEAT; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; RISK; SPECIES DIFFERENCE; TRANSMISSION; VIRULENCE;

LISTERIA MONOCYTOGENES;

BACTERIAL PROTEIN; HAND SANITIZER; INTERNALIN PROTEIN, BACTERIA; STOP CODON;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CODON, NONSENSE; COOKING AND EATING UTENSILS; DRUG RESISTANCE, BACTERIAL; FOODBORNE DISEASES; HAND SANITIZERS; HUMANS; INDIANA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEAT; MEAT PRODUCTS; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; RESTAURANTS; RISK; SPECIES SPECIFICITY; VIRULENCE;

EID: 84922436610     PISSN: 15353141     EISSN: 15567125     Source Type: Journal    
DOI: 10.1089/fpd.2014.1837     Document Type: Article

References (43)

1. Aase B, Sundheim G, Langsrud S, Rørvik LM. Occurrence of and a possible mechanism for resistance to a quaternary ammonium compound in Listeria monocytogenes. Int J Food Microbiol 2000;62:57-63.
2. Adrião A, Vieira M, Fernandes I, et al. Marked intra-strain variation in response of Listeria monocytogenes dairy isolates to acid or salt stress and the effect of acid or salt adaptation on adherence to abiotic surfaces. Int J Food Microbiol 2008;123:142-150.
3. Afzal Ghauri M, Okibe N, Barrie Johnson D. Attachment of acidophilic bacteria to solid surfaces: The significance of species and strain variations. Hydrometallurgy 2007;85:72-80.
4. Anonymous. FSIS comparative risk assessment for Listeria monocytogenes in ready-to-eat meat and poultry deli meats. 2010. Available at: http://www.fsis.usda.gov/shared/PDF/Comparative-RA-Lm-Report-May2010.pdf?redirecthttp= true, accessed June 11, 2014.
5. Borucki MK, Peppin JD, White D, Loge F, Call DR. Variation in biofilm formation among strains of Listeria monocytogenes. Appl Environ Microbiol 2003;69:7336-7342.
6. Chen J. Genetic and phenotypic characterization of Listeria monocytogenes from outbreaks, food, and food environments. [PhD dissertation]. Lubbock, TX: Texas Tech University, 2013.
7. Djordjevic D, Wiedmann M, McLandsborough L. Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied Environ Microbiol 2002;68:2950-2958.
8. Endrikat S, Gallagher D, Pouillot R, et al. A comparative risk assessment for Listeria monocytogenes in prepackaged versus retail-sliced deli meat. J Food Prot 2010;73:612-619.
9. Fraise A, Maillard J-Y, Sattar S. Russell, Hugo and Ayliffe's Principles and Practice of Disinfection, Preservation and Sterilization. Hoboken, NJ: John Wiley & Sons, 2012.
10. Frank JF, Koffi RA. Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to surfactant sanitizers and heat. J Food Prot 1990;53:550-554.
11. Furrer B, Candrian U, Hoefelein C, Luethy J. Detection and identification of Listeria monocytogenes in cooked sausage products and in milk by in vitro amplification of haemolysin gene fragments. J Appl Bacteriol 1991;70:372-379.
12. Gandhi M, Chikindas ML. Listeria: A foodborne pathogen that knows how to survive. Int J Food Microbiol 2007;113:1-15.
13. Gombas DE, Chen Y, Clavero RS, Scott VN. Survey of Listeria monocytogenes in ready-to-eat foods. J Food Prot 2003;66: 559-569.
14. Gray MJ, Zadoks RN, Fortes ED, et al. Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl Environ Microbiol 2004;70:5833-5841.
15. Heir E, Lindstedt B-A, Røtterud O-J, Vardund T, Kapperud G, Nesbakken T. Molecular epidemiology and disinfectant susceptibility of Listeria monocytogenes from meat processing plants and human infections. Int J Food Microbiol 2004;96:85-96.
16. Hoelzer K, Sauders BD, Sanchez MD, et al. Prevalence, distribution, and diversity of Listeria monocytogenes in retail environments, focusing on small establishments and establishments with a history of failed inspections. J Food Prot 2011;74:1083-1095.
17. Holah J, Taylor J, Dawson D, Hall K. Biocide use in the food industry and the disinfectant resistance of persistent strains of Listeria monocytogenes and Escherichia coli. J Appl Microbiol 2002;92:111S-120S.
18. Jacquet C, Doumith M, Gordon JI, Martin PM, Cossart P, Lecuit M. A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J Infect Dis 2004;189:2094-2100.
19. Lecuit M, Ohayon H, Braun L, Mengaud J, Cossart P. Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun 1997;65:5309-5319.
20. Lecuit M, Vandormael-Pournin S, Lefort J, et al. A transgenic model for listeriosis: Role of internalin in crossing the intestinal barrier. Science 2001;292:1722-1725.
21. Lemon KP, Higgins DE, Kolter R. Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 2007;189:4418-4424.
22. Lianou A, Sofos JN. A review of the incidence and transmission of Listeria monocytogenes in ready-to-eat products in retail and food service environments. J Food Prot 2007;70:2172-2198.
23. Lourenço A, Neves E, Brito L. Susceptibility of Listeria monocytogenes from traditional cheese-dairies to in-use sanitizers. Food Control 2009;20:585-589.
24. Lundén J, Autio T, Markkula A, Hellström S, Korkeala H. Adaptive and cross-adaptive responses of persistent and nonpersistent Listeria monocytogenes strains to disinfectants. Int J Food Microbiol 2003;82:265-272.
25. Lundén JM, Miettinen MK, Autio TJ, Korkeala HJ. Persistent Listeria monocytogenes strains show enhanced adherence to food contact surface after short contact times. J Food Prot 2000;63:1204-1207.
26. Mereghetti L, Quentin R, Marquet-Van Der Mee N, Audurier A. Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl Environ Microbiol 2000;66:5083-5086.
27. Neves E, Silva AC, Roche SM, Velge P, Brito L. Virulence of Listeria monocytogenes isolated from the cheese dairy environment, other foods and clinical cases. J Med Microbiol 2008;57:411-415.
28. Nightingale KK, Ivy RA, Ho AJ, et al. inlA premature stop codons are common among Listeria monocytogenes isolates from foods and yield virulence-attenuated strains that confer protection against fully virulent strains. Appl Environ Microbiol 2008;74:6570-6583.
29. Nightingale KK, Windham K, Martin KE, Yeung M, Wiedmann M. Select Listeria monocytogenes subtypes commonly found in foods carry distinct nonsense mutations in inlA, leading to expression of truncated and secreted internalin A, and are associated with a reduced invasion phenotype for human intestinal epithelial cells. Appl Environ Microbiol 2005;71:8764-8772.
30. Olier M, Pierre F, Rousseaux S, et al. Expression of truncated Internalin A is involved in impaired internalization of some Listeria monocytogenes isolates carried asymptomatically by humans. Infect Immun 2003;71:1217-1224.
31. Pan Y, Breidt F, Kathariou S. Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl Environ Microbiol 2006;72:7711-7717.
32. Poulsen LV. Microbial biofilm in food processing. LWT Food Sci Tech 1999;32:321-326.
33. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States-Major pathogens. Emerg Infect Dis 2011;17:7-15.
34. Simmons C, Stasiewicz MJ, Wright J, et al. Listeria monocytogenes and Listeria spp. contamination patterns in retail delicatessen establishments in three U.S. states. J Food Prot 2014;77:1929-1939.
35. Sofos JN. Biofilms: Our constant enemies. Foodsafety Mag 2009. Available at: http://www.foodsafetymagazine.com/magazine-archive1/februarymarch-2009/biofilms-our-constantenemies/, accessed June 11, 2014.
36. Sofos JN, Geornaras I. Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Escherichia coli O157: H7 in nonintact, and Listeria monocytogenes in ready-to-eat, meat products. Meat Sci 2010;86:2-14.
37. Soumet C, Ragimbeau C, Maris P. Screening of benzalkonium chloride resistance in Listeria monocytogenes strains isolated during cold smoked fish production. Lett Appl Microbiol 2005;41:291-296.
38. Tezel U, Pierson JA, Pavlostathis SG. Fate and effect of quaternary ammonium compounds on a mixed methanogenic culture. Water Res 2006;40:3660-3668.
39. To MS, Favrin S, Romanova N, Griffiths MW. Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Applied Environ Microbiol 2002;68:5258-5264.
40. Truelstrup Hansen L, Vogel BF. Desiccation of adhering and biofilm Listeria monocytogenes on stainless steel: Survival and transfer to salmon products. Int J Food Microbiol 2011;146:88-93.
41. Van Stelten A, Nightingale KK. Development and implementation of a multiplex single-nucleotide polymorphism genotyping assay for detection of virulence-attenuating mutations in the Listeria monocytogenes virulence-associated gene inlA. Appl Environ Microbiol 2008;74:7365-7375.
42. Van Stelten A, Simpson JM, Ward TJ, Nightingale KK. Revelation by single-nucleotide polymorphism genotyping that mutations leading to a premature stop codon in inlA are common among Listeria monocytogenes isolates from ready-to-eat foods but not human listeriosis cases. Appl Environ Microbiol 2010;76:2783-2790.
43. [WHO] World Health Organization. Risk Assessment of Listeria monocytogenes in Ready-to-Eat Foods. Washington, DC: WHO, 2004.