Early spoilage; Production batch recall; Psychrotrophic LAB; Leuconostoc gelidum subsp. gasicomitatum; 16S rRNA gene high-throughput sequencing
Abstract :
[en] Between 2010 and 2014 several spoilage cases in Belgium occurring in retail foodstuffs prior to the end of shelf-life have been reported to our laboratory. Overall, seven cases involved strictly psychrotrophic lactic acid bacteria (LAB) contamination in packaged and chilled-stored food products. The products derived either fromrecalls of entire production batches or as specimens of sporadic spoilage manifestations. Some of these samples were returned to the manufacturing companies by consumers who observed the alterations after purchasing the products. The products covered a wide range of foodstuffs (i.e. meat, dairy, vegetable, egg products and composite food) and denoted different spoilage defects. However, the microbiota determined by means of 16S rRNA gene high throughput sequencing analysis underpin few LAB genera (i.e. Leuconostoc, Lactobacillus, Weissella and Lactococcus), which are frequently encountered nowadays as specific spoilage organisms (SSO) albeit overlooked by mesophilic enumeration methods due to their strictly psychrotrophic character. The present study confirms the spreading of psychrotrophic LAB in Belgian food processing environments leading to unexpected spoilage, corroborating their spoilage dynamics and prevalence in all kinds of packaged and refrigerated foodstuffs in Northern Europe.
Disciplines :
Microbiology
Author, co-author :
Pothakos, Vasileios; Universiteit Gent - Ugent > Food Safety and Food Quality > Food Microbiology and Food Preservation
Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Huys, Geert; Universiteit Gent - Ugent > Faculty of Science > Laboratory of Microbiology and BCCM/LMG Bacteria Collection,
Nezer, Carine; Quality Partner sa
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Devlieghere, Frank; Universiteit Gent - Ugent > Food Safety and Food Quality > Food Microbiology and Food Preservation,
Language :
English
Title :
Psychrotrophic lactic acid bacteria associated with production batch recalls and sporadic cases of early spoilage in Belgium between 2010 and 2014
AFSCA, Agence Fédérale pour la Sécurité de la Chaîne Alimentaire AVIS 10-2012: Evaluation du document "Limites d' action pour les contaminants microbiologiques dans les denrées alimentaires" (dossier Sci Com 2011/21) 2012.
Allende A., Jacxsens L., Devlieghere F., Debevere J., Artés F. Effect of superatmospheric oxygen packaging on sensorial quality, spoilage, and Listeria monocytogenes and Aeromonas caviae growth in fresh processed mixed salads. J. Food Prot. 2002, 65(10):1565-1573.
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
Amanatidou A., Slump R.A., Gorris L.G.M., Smid E.J. High oxygen and high carbon dioxide modified atmospheres for shelf-life extension of minimally processed carrots. Food Chem. Toxicol. 2000, 65(1):61-66.
Audenaert K., D'Haene K., Messens K., Ruyssen T., Vandamme P., Huys G. Diversity of lactic acid bacteria from modified atmosphere packaged sliced cooked meat products at sell-by date assessed by PCR-denaturing gradient gel electrophoresis. Food Microbiol. 2010, 27(1):12-18.
Axelsson L. Lactic acid bacteria: classification and physiology. Lactic Acid Bacteria. Microbiological and Functional Aspects 2004, 1-66. Marcel Dekker, New York, NY, USA. Third Edition. S. Salminen, A. von Wright, A. Ouwehand (Eds.).
Björkroth J. Microbiological ecology of marinated meat products. Meat Sci. 2005, 70(3):477-480.
Björkroth J., Holzapfel W. Genera Leuconostoc, Oenococcus and Weissella. The Prokaryotes 2006, 267-319. Springer, New York, NY, USA. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt (Eds.).
Björkroth K.J., Geisen R., Schillinger U., Weiss N., De Vos P., Holzapfel W.H., Vandamme P. Characterization of Leuconostoc gasicomitatum sp. nov., associated with spoiled raw tomato-marinated broiler meat strips packaged under modified-atmosphere conditions. Appl. Environ. Microbiol. 2000, 66(9):3764-3772.
Borch E., Kant-Muermans M.L., Blixt Y. Bacterial spoilage of meat and cured meat products. Int. J. Food Microbiol. 1996, 33(1):103-120.
Brosius J., Dull T.J., Sleeter D.D., Noller H.F. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J. Mol. Biol. 1981, 148:107-127.
Cayré M., Garro O., Vignolo G. Effect of storage temperature and gas permeability of packaging film on the growth of lactic acid bacteria and in cooked meat emulsions. Food Microbiol. 2005, 22(6):505-512.
Chaillou S. Characterization of dynamic evolution of variable microbial spoilage components during storage of fresh meat and seafood products. Poster Session Presented at: 24th International ICFMH Conference, Food Micro 2014; 2014 1-4 Sep; Nantes, FR 2014.
Chao A., Bunge J. Estimating the number of species in a stochastic abundance model. Biometrics 2002, 58(3):531-539.
Chao A., Shen T.-J. Nonparametric estimation of Shannon's index of diversity when there are unseen species in sample. Environ. Ecol. Stat. 2003, 10:429-443.
Colwell R.K., Coddington J.A. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. R. Soc. Lond. 1994, 345(1311):101-118.
Dainty R.H., Mackey B.M. The relationship between the phenotypic properties of bacteria from chill-stored meat and spoilage processes. Soc. Appl. Bacteriol. Symp. Ser. 1992, 21:103-114.
De Filippis F., La Storia A., Villani F., Ercolini D. Exploring the sources of bacterial spoilers in beefsteaks by culture-independent high-throughput sequencing. PLoS One 2013, 8:1-10.
Di Bella J.M., Bao Y., Gloor G.B., Burton J.P., Reid G. High throughput sequencing methods and analysis for microbiome research. J. Microbiol. Methods 2013, 10.1016/j.mimet.2013.08.011.
Ercolini D. High-throughput sequencing and metagenomics: moving forward in the culture-independent analysis of food microbial ecology. Appl. Environ. Microbiol. 2013, 79(10):3148-3155.
Ercolini D., Russo F., Nasi A., Ferranti P., Villani F. Mesophilic and psychrotrophic bacteria from meat and their spoilage potential in vitro and in beef. Appl. Environ. Microbiol. 2009, 75(7):1990-2001.
Ercolini D., Casaburi A., Nasi A., Ferrocino I., Di Monaco R., Ferranti P., Mauriello G., Villani F. Different molecular types of Pseudomonas fragi have the same overall behaviour as meat spoilers. Int. J. Food Microbiol. 2010, 142:120-131.
Franz C.M.A.P., Holzapfel W.H. Chapter 1: the importance of understanding the stress physiology of lactic acid bacteria. Stress Responses of Lactic Acid Bacteria 2011, 3-20. Springer US, Boston, MA. E. Tsakalidou, K. Papadimitriou (Eds.).
Geysen S., Geeraerd A.H., Verlinden B.E., Michiels C.W., Van Impe J.F., Nicolaï B.M. Predictive modelling and validation of Pseudomonas fluorescens growth at superatmospheric oxygen and carbon dioxide concentrations. Food Microbiol. 2005, 22(2):149-158.
Gómez-López V.M., Ragaert P., Ryckeboer J., Jeyachchandran V., Debevere J., Devlieghere F. Shelf-life of minimally processed cabbage treated with neutral electrolysed oxidising water and stored under equilibrium modified atmosphere. Int. J. Food Microbiol. 2007, 117(1):91-98.
Gould G.W. Methods for preservation and extension of shelf life. Int. J. Food Microbiol. 1996, 33:51-64.
Haas B.J., Gevers D., Earl A.M., Feldgarden M., Ward D.V., Giannoukos G., Birren B.W. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 2011, 21(3):494-504.
Holley R.a, McKellar R.C. Influence of unsliced delicatessen meat freshness upon bacterial growth in subsequently prepared vacuum packed slices. Int. J. Food Microbiol. 1996, 29:297-309.
Kato Y., Sakala R.M., Hayashidani H., Kiuchi A., Kaneuchi C., Ogawa M. Lactobacillus algidus sp. nov., a psychrophilic lactic acid bacterium isolated from vacuum-packaged refrigerated beef. Int. J. Syst. Evol. Microbiol. 2000, 50:1143-1149.
Li Y., Brackett R.E., Shewfelt R.L., Beuchat L.R. Changes in appearance and natural microflora on iceberg lettuce treated in warm, chlorinated water and then stored at refrigeration temperature. Food Microbiol. 2001, 18(3):299-308.
Lyhs U., Björkroth J.K. Lactobacillus sakei/curvatus is the prevailing lactic acid bacterium group in spoiled maatjes herring. Food Microbiol. 2008, 25(3):529-533.
Lyhs U., Lahtinen J., Fredriksson-Ahomaa M., Hyytiä-Trees E., Elfing K., Korkeala H. Microbiological quality and shelf-life of vacuum-packaged "gravad" rainbow trout stored at 3 and 8°C. Int. J. Food Microbiol. 2001, 70:221-230.
Lyhs U., Korkeala H., Björkroth J. Identification of lactic acid bacteria from spoiled, vacuum-packaged "gravad" rainbow trout using ribotyping. Int. J. Food Microbiol. 2002, 72:147-153.
Lyhs U., Koort J., Lundström H.-S., Björkroth K.J. Leuconostoc gelidum and Leuconostoc gasicomitatum strains dominated the lactic acid bacterium population associated with strong slime formation in an acetic-acid herring preserve. Int. J. Food Microbiol. 2004, 90(2):207-218.
Newcombe R.G. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat. Med. 1998, 17:857-872.
Nieminen T.T., Vihavainen E., Paloranta A., Lehto J., Paulin L., Auvinen P., Björkroth K.J. Characterization of psychrotrophic bacterial communities in modified atmosphere-packed meat with terminal restriction fragment length polymorphism. Int. J. Food Microbiol. 2011, 144(3):360-366.
Nychas G., Skandamis P., Tassou C., Koutsoumanis K. Meat spoilage during distribution. Meat Sci. 2008, 78:77-89.
Pothakos V., Samapundo S., Devlieghere F. Total mesophilic counts underestimate in many cases the contamination levels of psychrotrophic lactic acid bacteria (LAB) in chilled-stored food products at the end of their shelf-life. Food Microbiol. 2012, 32(2):437-443.
Pothakos V., Snauwaert C., De Vos P., Huys G., Devlieghere F. Psychrotrophic members of Leuconostoc gasicomitatum, Leuconostoc gelidum and Lactococcus piscium dominate at the end of shelf-life in packaged and chilled-stored food products in Belgium. Food Microbiol. 2014, 39:61-67.
Pothakos V., Snauwaert C., De Vos P., Huys G., Devlieghere F. Monitoring psychrotrophic lactic acid bacteria contamination in a ready-to-eat vegetable salad production environment. Int. J. Food Microbiol. 2014, 185:7-16.
Pothakos V., Nyambi C., Zhang B.-Y., Papastergiadis A., De Meulenaer B., Devlieghere F. Spoilage potential of psychrotrophic lactic acid bacteria (LAB) species: Leuconostoc gelidum subsp. gasicomitatum and Lactococcus piscium, on sweet bell pepper (SBP) simulation medium under different gas compositions. Int. J. Food Microbiol. 2014, 178:120-129.
Pruesse E., Quast C., Knittel K., Fuchs B.M., Ludwig W., Peplies J., Glöckner F.O. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35(21):7188-7196.
Rahkila R., Johansson P., Säde E., Björkroth J. Identification of enterococci from broiler products and a broiler processing plant and description of Enterococcus viikkiensis sp. nov. Appl. Environ. Microbiol. 2011, 77(4):1196-1203.
Rivals I., Personnaz L., Taing L., Potier M.-C. Enrichment or depletion of a GO category within a class of genes: which test?. Bioinformatics 2007, 23(4):401-407.
Säde E. Leuconostoc spoilage of refrigerated, packaged foods. Veterinary Medicine 2011, University of Helsinki.
Sakala R.M., Hayashidani H., Kato Y., Kaneuchi C., Ogawa M. Isolation and characterization of Lactococcus piscium strains from vacuum-packaged refrigerated beef. J. Appl. Microbiol. 2002, 92(1):173-179.
Sakala R.M., Kato Y., Hayashidani H., Murakami M., Kaneuchi C., Ogawa M. Lactobacillus fuchuensis sp. nov., isolated from vacuum-packaged refrigerated beef. Int. J. Syst. Evol. Microbiol. 2002, 52:1151-1154.
Samelis J., Kakouri A., Rementzis J. The spoilage microflora of cured, cooked turkey breasts prepared commercially with or without smoking. Int. J. Food Microbiol. 2000, 56(2-3):133-143.
Santos E.M., Jaime I., Rovira J., Lyhs U., Korkeala H., Björkroth J. Characterization and identification of lactic acid bacteria in "morcilla de Burgos". Int. J. Food Microbiol. 2005, 97(3):285-296.
Schirmer B.C., Heir E., Langsrud S. Characterization of the bacterial spoilage flora in marinated pork products. J. Appl. Microbiol. 2009, 106(6):2106-2116.
Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Weber C.F. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75(23):7537-7541.
Sidhu M.S., Langsrud S., Holck A. Disinfectant and antibiotic resistance of lactic acid bacteria isolated from the food industry. Microb. Drug Resist. 2001, 7(1):73-83.
Temple T.N., Toit L.J., Derie M.L., Johnson K.B. Quantitative molecular detection of Xanthomonas hortorum pv. carotae in carrot seed before and after hot-water treatment. Plant Dis. 2013, 97(12):1585-1592.
Uyttendaele M., Jacxsens L., De Loy-Hendrickx A., Devlieghere F., Debevere J. Microbiologische richtwaarden & wettelijke microbiologische criteria (Labo levensmiddelenmicrobiologie en conservering, Universiteit Gent) 2010.
Vasilopoulos C., Ravyts F., De Maere H., De Mey E., Paelinck H., De Vuyst L., Leroy F. Evaluation of the spoilage lactic acid bacteria in modified-atmosphere-packaged artisan-type cooked ham using culture-dependent and culture-independent approaches. J. Appl. Microbiol. 2008, 104(5):1341-1353.
Vasilopoulos C., De Maere H., De Mey E., Paelinck H., De Vuyst L., Leroy F. Technology-induced selection towards the spoilage microbiota of artisan-type cooked ham packed under modified atmosphere. Food Microbiol. 2010, 27(1):77-84.
Vihavainen E.J., Björkroth K.J. Spoilage of value-added, high-oxygen modified-atmosphere packaged raw beef steaks by Leuconostoc gasicomitatum and Leuconostoc gelidum. Int. J. Food Microbiol. 2007, 119(3):340-345.
Vihavainen E.J., Murros A.E., Björkroth K.J. Leuconostoc spoilage of vacuum-packaged vegetable sausages. J. Food Prot. 2008, 71(11):2312-2315.
Wang Y., Qian P.-Y. Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 2009, 4(10):1-9.
Welch R.W., Mitchell P.C. Food processing: a century of change. Br. Med. Bull. 2000, 56(1):1-17.
Zhang B.-Y., Samapundo S., Pothakos V., Sürengil G., Devlieghere F. Effect of high oxygen and high carbon dioxide atmosphere packaging on the microbial spoilage and shelf-life of fresh-cut honeydew melon. Int. J. Food Microbiol. 2013, 166(3):378-390.
