The use of multiplex PCR to detect and differentiate food- and beverage-associated microorganisms: a review.

Regarding food safety, rapid detection of microbial species is crucial to develop effective preventive and/or adjustment measures. Classical methods for determining the presence of certain species are time-consuming and labor-intensive, hence, molecular methods, which offer speed, sensitivity and specificity, have been developed to address this problem. Multiplex PCR (MPCR) is widely applied in the various fields of microbiology for the rapid differentiation of microbial species without compromising accuracy. This paper describes the method and reports on the state-of-the-art application of this technique to the identification of microorganisms vehiculated with foods and beverages. The identification of both pathogens and probiotics and the species important for food fermentation or deterioration will be discussed. Applications of MPCR in combination with other techniques are also reviewed. Potentials, pitfalls, limitations and future prospects are summarised.

[1]  J. Osek Rapid and specific identification of Shiga toxin‐producing Escherichia coli in faeces by multiplex PCR , 2002, Letters in applied microbiology.

[2]  Dm Jones Recent Advances in Streptococci and Streptococcal Diseases , 1986 .

[3]  M. Alam,et al.  Arcobacter halophilus sp. nov., the first obligate halophile in the genus Arcobacter. , 2005, International journal of systematic and evolutionary microbiology.

[4]  J. Osek Development of a multiplex PCR approach for the identification of Shiga toxin‐producing Escherichia coli strains and their major virulence factor genes , 2003, Journal of applied microbiology.

[5]  J. Musser,et al.  Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[6]  O. Sethabutr,et al.  Development of a ceuE-based multiplex polymerase chain reaction (PCR) assay for direct detection and differentiation of Campylobacter jejuni and Campylobacter coli in Thailand. , 2001, Diagnostic microbiology and infectious disease.

[7]  J. Songer,et al.  Genotyping ofClostridium perfringensby Polymerase Chain Reaction is a Useful Adjunct to Diagnosis of Clostridial Enteric Disease in Animals , 1996 .

[8]  M. Karmali,et al.  Infection by verocytotoxin-producing Escherichia coli , 1989, Clinical Microbiology Reviews.

[9]  S. Stampi,et al.  Prevalence of thermophilic Campylobacter and Arcobacter butzleri in food of animal origin. , 1996, International journal of food microbiology.

[10]  J. Lim,et al.  Comparison of vancomycin-resistant enterococci isolates from human, poultry and pigs in Korea. , 2005, Veterinary microbiology.

[11]  M. Gottschalk,et al.  Molecular serotype identification of Streptococcus agalactiae of bovine origin by multiplex PCR-based reverse line blot (mPCR/RLB) hybridization assay. , 2006, FEMS microbiology letters.

[12]  Ann Croft,et al.  Description of a multiplex Bordetella pertussis and Bordetella parapertussis LightCycler PCR assay with inhibition control. , 2003, Diagnostic microbiology and infectious disease.

[13]  H. Lior,et al.  A new heat-labile cytolethal distending toxin (CLDT) produced by Escherichia coli isolates from clinical material. , 1988, Microbial pathogenesis.

[14]  E. Lee,et al.  Nonfatal and fatal infections caused by Chromobacterium violaceum. , 1993, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[15]  P. Vandamme,et al.  Arcobacter cibarius sp. nov., isolated from broiler carcasses. , 2005, International journal of systematic and evolutionary microbiology.

[16]  Robin Patel,et al.  Multiplex LightCycler PCR Assay for Detection and Differentiation of Bordetella pertussis and Bordetella parapertussis in Nasopharyngeal Specimens , 2002, Journal of Clinical Microbiology.

[17]  A. Cifuentes,et al.  Quantitation of transgenic Bt event-176 maize using double quantitative competitive polymerase chain reaction and capillary gel electrophoresis laser-induced fluorescence. , 2004, Analytical chemistry.

[18]  Naresh K. Sharma,et al.  Development of a Single-Reaction Multiplex PCR Toxin Typing Assay for Staphylococcus aureusStrains , 2000, Applied and Environmental Microbiology.

[19]  C. Buchrieser,et al.  Pulsed-field gel electrophoresis applied for comparing Listeria monocytogenes strains involved in outbreaks. , 1993, Canadian journal of microbiology.

[20]  Daniel D. Jones,et al.  Detection of Microbial Pathogens in Shellfish with Multiplex PCR , 1998, Current Microbiology.

[21]  Y. Park,et al.  Molecular typing and epidemiological survey of prevalence of Clostridium perfringens types by multiplex PCR , 1997, Journal of clinical microbiology.

[22]  P. Hsueh,et al.  Bacteremia caused by Arcobacter cryaerophilus 1B , 1997, Journal of clinical microbiology.

[23]  J. Kur,et al.  Differentiation of seventeen genospecies of Acinetobacter by multiplex polymerase chain reaction and restriction fragment length polymorphism analysis. , 1996, Molecular and cellular probes.

[24]  W. D. de Vos,et al.  Diversity, vitality and activities of intestinal lactic acid bacteria and bifidobacteria assessed by molecular approaches. , 2005, FEMS microbiology reviews.

[25]  R. Fuller Probiotics : the scientific basis , 1992 .

[26]  J. Terajima,et al.  Multiplex polymerase chain reaction assay for selective detection of Salmonella enterica serovar typhimurium. , 2003, Japanese journal of infectious diseases.

[27]  J. Farber,et al.  Molecular strategies for the detection, identification, and differentiation between enteroinvasive Escherichia coli and Shigella spp. , 2005, Journal of food protection.

[28]  M. Popoff,et al.  Typing of sheep clinical isolates and identification of enterotoxigenic Clostridium perfringens strains by classical methods and by polymerase chain reaction (PCR). , 1999, FEMS immunology and medical microbiology.

[29]  I. Chinen,et al.  Multiplex PCR Assay for Identification of Human Diarrheagenic Escherichia coli , 2003, Journal of Clinical Microbiology.

[30]  P. Gerner-Smidt,et al.  Multicenter validation of a multiplex PCR assay for differentiating the major Listeria monocytogenes serovars 1/2a, 1/2b, 1/2c, and 4b: toward an international standard. , 2005, Journal of food protection.

[31]  N. French,et al.  Occurrence of Clostridium perfringens β2-toxin amongst animals, determined using genotyping and subtyping PCR assays , 2000, Epidemiology and Infection.

[32]  K. Prasad,et al.  Campylobacter species associated with diarrhoea in patients from a tertiary care centre of north India. , 2001, The Indian journal of medical research.

[33]  F. Clifton-Hadley Detection and diagnosis of Escherichia coli O157 and other verocytotoxigenic E. coli in animal faeces , 2000 .

[34]  K. Yamaguchi,et al.  Multiplex PCR for the simultaneous detection of Chlamydia pneumoniae, Mycoplasma pneumoniae and Legionella pneumophila in community-acquired pneumonia. , 2004, Respiratory medicine.

[35]  H. Dockrell,et al.  Use of polymerase chain reaction to assess efficacy of leprosy chemotherapy , 1993, The Lancet.

[36]  幸雄 森田,et al.  Arcobacter butzleriとA. cryaerophilusの分離・同定法の検討ならびに鶏肉の汚染状況 , 2001 .

[37]  J. Morris,et al.  Emerging foodborne pathogens: Escherichia coli O157:H7 as a model of entry of a new pathogen into the food supply of the developed world. , 1996, Epidemiologic reviews.

[38]  M. Rowe,et al.  A PCR assay for the detection of Campylobacter jejuni and Campylobacter coli in water , 1994, Letters in applied microbiology.

[39]  Insook Son,et al.  Prevalence of Arcobacter and Campylobacter on broiler carcasses during processing. , 2007, International journal of food microbiology.

[40]  C. Parker,et al.  Differentiation of Campylobacter coli, Campylobacter jejuni, Campylobacter lari, and Campylobacter upsaliensis by a Multiplex PCR Developed from the Nucleotide Sequence of the Lipid A Gene lpxA , 2004, Journal of Clinical Microbiology.

[41]  G. Vignolo,et al.  Direct Molecular Approach to Monitoring Bacterial Colonization on Vacuum-Packaged Beef , 2006, Applied and Environmental Microbiology.

[42]  M. Gobbetti,et al.  Characterization of Non-Starter Lactic Acid Bacteria from Italian Ewe Cheeses Based on Phenotypic, Genotypic, and Cell Wall Protein Analyses , 2001, Applied and Environmental Microbiology.

[43]  P. Vandamme,et al.  Development of a multiplex PCR assay for the simultaneous detection and identification of Arcobacter butzleri, Arcobacter cryaerophilus and Arcobacter skirrowii. , 2000, FEMS microbiology letters.

[44]  M. Wiedmann,et al.  Combined sigB allelic typing and multiplex PCR provide improved discriminatory power and reliability for Listeria monocytogenes molecular serotyping. , 2007, Journal of microbiological methods.

[45]  L. Aquilanti,et al.  Resident lactic acid bacteria in raw milk Canestrato Pugliese cheese , 2006, Letters in applied microbiology.

[46]  B. Swaminathan,et al.  9 Subtyping Listeria monocytogenes , 2007 .

[47]  E. Louis,et al.  Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae. , 2000, International journal of systematic and evolutionary microbiology.

[48]  D. van Sinderen,et al.  Rapid Differentiation and In Situ Detection of 16 Sourdough Lactobacillus Species by Multiplex PCR , 2005, Applied and Environmental Microbiology.

[49]  L. Vrijmoed,et al.  Co-detection of three species of water-borne bacteria by multiplex PCR , 1995 .

[50]  Effect of iron limitation on protein composition and ultrastructure of Haemophilus ducreyi. , 1990, FEMS microbiology letters.

[51]  U. Schotte,et al.  Diagnostic multiplex PCR for toxin genotyping of Clostridium perfringens isolates. , 2004, Veterinary microbiology.

[52]  R. Harvey,et al.  Prevalence of Campylobacter, Salmonella, and Arcobacter species at slaughter in market age pigs. , 1999, Advances in experimental medicine and biology.

[53]  J. Paton,et al.  Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. , 1998, Journal of clinical microbiology.

[54]  J. Coia,et al.  Clinical, microbiological and epidemiological aspects of Escherichia coli O157 infection , 2006 .

[55]  M. Kaufmann,et al.  Identification of Acinetobacter baumannii by Detection of the blaOXA-51-like Carbapenemase Gene Intrinsic to This Species , 2006, Journal of Clinical Microbiology.

[56]  Elie. Metchnikoff The Prolongation of Life: Optimistic Studies , 2003 .

[57]  J. Tappero Reduction in the incidence of human listeriosis in the United States , 1995 .

[58]  J. Coia MiniReviewClinical, microbiological and epidemiological aspects of Escherichia coli O157 infection , 1998 .

[59]  E. Augustynowicz,et al.  Molecular epidemiology survey of toxinogenic Clostridium perfringens strain types by multiplex PCR. , 2000, Scandinavian journal of infectious diseases.

[60]  R. Jones Observations on the succession dynamics of lactic acid bacteria populations in chill-stored vacuum-packaged beef. , 2004, International journal of food microbiology.

[61]  S. Fujimoto,et al.  Multiplex PCR for Detection of Genes for Staphylococcus aureus Enterotoxins , 2002 .

[62]  E. Gallagher,et al.  Mechanisms of aflatoxin carcinogenesis. , 1994, Annual review of pharmacology and toxicology.

[63]  M. Griffiths,et al.  Isolation and characterization of Carnobacterium, Lactococcus, and Enterococcus spp. from cooked, modified atmosphere packaged, refrigerated, poultry meat. , 2000, International journal of food microbiology.

[64]  R. Vogel,et al.  Characterization of the bacterial flora of Sudanese sorghum flour and sorghum sourdough , 1997, Journal of applied microbiology.

[65]  J. Guyot,et al.  Polyphasic Study of the Spatial Distribution of Microorganisms in Mexican Pozol, a Fermented Maize Dough, Demonstrates the Need for Cultivation-Independent Methods To Investigate Traditional Fermentations , 1999, Applied and Environmental Microbiology.

[66]  Daniel B. Oerther,et al.  The oligonucleotide probe database , 1996, Applied and environmental microbiology.

[67]  Ji-Yeon Kim,et al.  Isolation and identification of Escherichia coli O157:H7 using different detection methods and molecular determination by multiplex PCR and RAPD. , 2005, Journal of veterinary science.

[68]  R. Amann,et al.  The species concept for prokaryotes. , 2013, FEMS microbiology reviews.

[69]  Gehua Wang,et al.  Colony Multiplex PCR Assay for Identification and Differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus , 2002, Journal of Clinical Microbiology.

[70]  D. van Sinderen,et al.  Combination of Multiplex PCR and PCR-Denaturing Gradient Gel Electrophoresis for Monitoring Common Sourdough-Associated Lactobacillus Species , 2006, Applied and Environmental Microbiology.

[71]  G. Peters,et al.  Rapid and Specific Detection of Toxigenic Staphylococcus aureus: Use of Two Multiplex PCR Enzyme Immunoassays for Amplification and Hybridization of Staphylococcal Enterotoxin Genes, Exfoliative Toxin Genes, and Toxic Shock Syndrome Toxin 1 Gene , 1998, Journal of Clinical Microbiology.

[72]  A. Gafni,et al.  Effect of routine use of a multiplex PCR for detection of vanA- and vanB- mediated enterococcal resistance on accuracy, costs and earlier reporting. , 2001, Diagnostic microbiology and infectious disease.

[73]  R. Tauxe,et al.  Salmonella surveillance: a global survey of public health serotyping , 2002, Epidemiology and Infection.

[74]  M. Ventura,et al.  Specific Identification and Targeted Characterization ofBifidobacterium lactis from Different Environmental Isolates by a Combined Multiplex-PCR Approach , 2001, Applied and Environmental Microbiology.

[75]  K. Holmes,et al.  Prevalence and characterization of hippurate-negative Campylobacter jejuni in King County, Washington , 1987, Journal of clinical microbiology.

[76]  T. Koivula,et al.  A HUMAN LACTOBACILLUS STRAIN (LACTOBACILLUS GG) PROMOTES RECOVERY FROM ACUTE DIARRHOEA IN CHILDREN , 1990, Pediatric Research.

[77]  M. Wagner,et al.  Development of a multiplex and semi-nested PCR assay for detection of Yersinia enterocolitica and Aeromonas hydrophila in raw milk , 2000 .

[78]  C. Buchrieser,et al.  Differentiation of the Major Listeria monocytogenes Serovars by Multiplex PCR , 2004, Journal of Clinical Microbiology.

[79]  B. Pot,et al.  The genus Enterococcus , 1995 .

[80]  Paul M. Orwin,et al.  Characterization of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. , 2002, Biochemistry.

[81]  P. Fox,et al.  Characterization of sourdough lactic acid bacteria based on genotypic and cell-wall protein analyses. , 2003, Journal of applied microbiology.

[82]  I. Wesley,et al.  Detection of Arcobacter spp. in Ground Pork by Modified Plating Methods. , 1996, Journal of food protection.

[83]  C. Phillips Incidence, epidemiology and prevention of foodborne Campylobacter species , 1995 .

[84]  C. Bezuidenhout,et al.  Multiplex PCR‐based detection of potential fumonisin‐producing Fusarium in traditional African vegetables , 2006, Environmental toxicology.

[85]  R. Brosch,et al.  Pulsed-field fingerprinting of listeriae: identification of genomic divisions for Listeria monocytogenes and their correlation with serovar , 1994, Applied and environmental microbiology.

[86]  G. Browning,et al.  Multiplex polymerase chain reaction assay for simultaneous detection of Staphylococcus aureus and streptococcal causes of bovine mastitis. , 2001, Journal of dairy science.

[87]  R. Moellering Emergence of Enterococcus as a significant pathogen. , 1992, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[88]  G R Gibson,et al.  Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. , 1995, The Journal of nutrition.

[89]  J. A. Koburger,et al.  Isolation of Chromobacterium spp. from foods, soil, and water , 1982, Applied and environmental microbiology.

[90]  R. Vogel,et al.  Development and potential of starter lactobacilli resulting from exploration of the sourdough ecosystem , 2002, Antonie van Leeuwenhoek.

[91]  J. Mahony,et al.  Direct detection of vanA and vanB genes in clinical specimens for rapid identification of vancomycin resistant enterococci (VRE) using multiplex PCR. , 1999, Molecular and cellular probes.

[92]  J. Jonasson,et al.  Identification of mixed bacterial DNA contamination in broad-range PCR amplification of 16S rDNA V1 and V3 variable regions by pyrosequencing of cloned amplicons. , 2003, FEMS microbiology letters.

[93]  W. Goebel,et al.  Detection and Differentiation ofListeria spp. by a Single Reaction Based on Multiplex PCR , 1999, Applied and Environmental Microbiology.

[94]  E. Singer,et al.  Multiplex PCR using 16S rRNA gene-targeted primers for the identification of bifidobacteria from human origin. , 2003, FEMS microbiology letters.

[95]  W. Goebel,et al.  Listeria Pathogenesis and Molecular Virulence Determinants , 2001, Clinical Microbiology Reviews.

[96]  T. Mikami,et al.  One-step polymerase chain reaction-based typing of Arcobacter species. , 2003, International journal of food microbiology.

[97]  S. Kresovich,et al.  DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. , 1992, Nucleic acids research.

[98]  C. Lämmler,et al.  Multiplex polymerase chain reaction for identification and differentiation of Streptococcus equi subsp. zooepidemicus and Streptococcus equi subsp. equi. , 2004, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[99]  B. Murray The life and times of the Enterococcus , 1990, Clinical Microbiology Reviews.

[100]  H. Lee,et al.  Multiplex PCR-based detection and identification of Leuconostoc species. , 2000, FEMS microbiology letters.

[101]  Y. G. Kim,et al.  Detection of Escherichia coli O157:H7, Salmonella spp., Staphylococcus aureus and Listeria monocytogenes in kimchi by multiplex polymerase chain reaction (mPCR). , 2006, Journal of microbiology.

[102]  G. Stelma,et al.  Direct Polymerase Chain Reaction Detection of Campylobacter jejuni and Campylobacter coli in Raw Milk and Dairy Products , 1993, Applied and environmental microbiology.

[103]  B. Mackey,et al.  Effect of stress treatments on the detection of Listeria monocytogenes and enterotoxigenic Escherichia coli by the polymerase chain reaction. , 1994, The Journal of applied bacteriology.

[104]  L. Fox,et al.  Characterization of staphylococcal bovine mastitis isolates using the polymerase chain reaction. , 1998, Journal of food protection.

[105]  A. Cifuentes,et al.  Detection and differentiation of several food-spoilage lactic acid bacteria by multiplex polymerase chain reaction, capillary gel electrophoresis, and laser-induced fluorescence. , 2004, Journal of Agricultural and Food Chemistry.

[106]  V. Cardile,et al.  Research Section DNA damage in human fibroblasts exposed to fumonisin B1 , 2002 .

[107]  Seonghan Kim,et al.  Multiplex PCR-Based Method for Identification of Common Clinical Serotypes of Salmonella enterica subsp. enterica , 2006, Journal of Clinical Microbiology.

[108]  C. Yost,et al.  The use of multiplex PCR reactions to characterize populations of lactic acid bacteria associated with meat spoilage , 2000, Letters in applied microbiology.

[109]  M. Wiedmann Molecular subtyping methods for Listeria monocytogenes. , 2002, Journal of AOAC International.

[110]  B. China,et al.  Typing of bovine attaching and effacing Escherichia coli by multiplex in vitro amplification of virulence-associated genes , 1996, Applied and environmental microbiology.

[111]  R. Kong,et al.  Rapid detection of six types of bacterial pathogens in marine waters by multiplex PCR. , 2002, Water research.

[112]  S. Ricke,et al.  Vancomycin-resistant enterococci from nosocomial, community, and animal sources in the United States , 1996, Antimicrobial agents and chemotherapy.

[113]  Kunitomo Watanabe,et al.  Rapid identification of 11 human intestinal Lactobacillus species by multiplex PCR assays using group- and species-specific primers derived from the 16S-23S rRNA intergenic spacer region and its flanking 23S rRNA. , 2000, FEMS microbiology letters.

[114]  Carl A. Batt,et al.  Encyclopedia of Food Microbiology , 2000 .

[115]  C. Woloshuk,et al.  Multiplex real-time PCR detection of fumonisin-producing and trichothecene-producing groups of Fusarium species. , 2004, Journal of food protection.

[116]  S. Torriani,et al.  Differentiation of Lactobacillus plantarum,L. pentosus, and L. paraplantarum by recA Gene Sequence Analysis and Multiplex PCR Assay with recA Gene-Derived Primers , 2001, Applied and Environmental Microbiology.

[117]  P. Fedorka-Cray,et al.  Use of a Genus- and Species-Specific Multiplex PCR for Identification of Enterococci , 2004, Journal of Clinical Microbiology.

[118]  J. Pitt,et al.  The source of ochratoxin A in Brazilian coffee and its formation in relation to processing methods. , 2003, International journal of food microbiology.

[119]  G. Vignolo,et al.  The control of Listeria innocua and Lactobacillus sakei in broth and meat slurry with the bacteriocinogenic strain Lactobacillus casei CRL705 , 2004 .

[120]  R M Atlas,et al.  Effect of amplicon size on PCR detection of bacteria exposed to chlorine. , 1993, PCR methods and applications.

[121]  R. Reporter,et al.  Campylobacter upsaliensis: Another pathogen for consideration in the United States. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[122]  R. Jones,et al.  Evaluation of Vitek and API 20S for species identification of enterococci. , 1995, Diagnostic microbiology and infectious disease.

[123]  L. Settanni,et al.  Lactobacilli in sourdough fermentation , 2007 .

[124]  C. Cerniglia,et al.  Occurrence of non-O157 shiga toxin-producing Escherichia coli in ready-to-eat food from supermarkets in Argentina. , 2006, Food microbiology.

[125]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[126]  K. Kobayashi,et al.  Enzyme-linked immunosorbent assay for rapid detection of toxins from Clostridium perfringens. , 1991, FEMS microbiology letters.

[127]  G. Daube,et al.  Typing of Clostridium perfringens by in vitro amplification of toxin genes. , 1994, The Journal of applied bacteriology.

[128]  É. Oswald,et al.  Detection of the cytolethal distending toxin locus cdtB among diarrheagenic Escherichia coli isolates from humans in Iran. , 2005, Research in microbiology.

[129]  M. Drake,et al.  Development of a multiplex polymerase chain reaction assay for detection and differentiation of Staphylococcus aureus in dairy products. , 2001, Journal of food protection.

[130]  Robert V. Tauxe,et al.  Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations , 2000 .

[131]  M. Altwegg,et al.  Development of a multiplex real-time quantitative PCR assay to detect Chlamydia pneumoniae, Legionella pneumophila and Mycoplasma pneumoniae in respiratory tract secretions. , 2003, Diagnostic microbiology and infectious disease.

[132]  L. Morelli,et al.  Selective detection, enumeration and identification of potentially probiotic Lactobacillus and Bifidobacterium species in mixed bacterial populations. , 1997, International journal of food microbiology.

[133]  É. Oswald,et al.  Characteristics of cytotoxic necrotizing factor and cytolethal distending toxin producing Escherichia coli strains isolated from meat samples in Northern Ireland. , 2006, Food microbiology.

[134]  J. Langhendries,et al.  Effect of a fermented infant formula containing viable bifidobacteria on the fecal flora composition and pH of healthy full-term infants. , 1995, Journal of pediatric gastroenterology and nutrition.

[135]  L. Gram,et al.  Microbiological spoilage of fish and fish products. , 1996, International journal of food microbiology.

[136]  M. Collins,et al.  Phylogenetic analysis of the genus Lactobacillus and related lactic acid bacteria as determined by reverse transcriptase sequencing of 16S rRNA , 1991 .

[137]  I. Peiris Listeria monocytogenes, a Food-Borne Pathogen , 1991, Microbiological reviews.

[138]  P. Hagedorn,et al.  Rapid Identification and Differentiation of Clinical Isolates of Enteropathogenic Escherichia coli (EPEC), Atypical EPEC, and Shiga Toxin-Producing Escherichia coli by a One-Step Multiplex PCR Method , 2006, Journal of Clinical Microbiology.

[139]  J. Hamilton-miller,et al.  Identification of clinically isolated vancomycin-resistant enterococci: comparison of API and BBL Crystal systems. , 1999, Journal of medical microbiology.

[140]  R. Yolken,et al.  Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus , 1994, The Lancet.

[141]  L. Morelli,et al.  Specific detection of a probiotic Lactobacillus strain in faecal samples by using multiplex PCR. , 1998, FEMS microbiology letters.

[142]  A. Chandrashekar,et al.  PCR-restriction fragment length analysis of aflR gene for differentiation and detection of Aspergillus flavus and Aspergillus parasiticus in maize. , 2004, International journal of food microbiology.

[143]  R A Gibbs,et al.  Deletion screening of the Duchenne muscular dystrophy locus via multiplex DNA amplification. , 1988, Nucleic acids research.

[144]  P. Davidson,et al.  Growth and Production of Enterotoxin A by Staphylococcus aureus on "Home-style" French Fries , 1999 .

[145]  G. Daube,et al.  Prevalence of enterohaemorrhagic Escherichia coli from serotype O157 and other attaching and effacing Escherichia coli on bovine carcasses in Algeria , 2006, Journal of applied microbiology.

[146]  W. Jung,et al.  Application of extended single-reaction multiplex polymerase chain reaction for toxin typing of Staphylococcus aureus isolates in South Korea. , 2004, International journal of food microbiology.

[147]  P. Tarr Escherichia coli 0157:H7: Clinical, Diagnostic, and Epidemiological Aspects of Human Infection , 1995 .

[148]  R. Vogel,et al.  Multiplex PCR for the Detection ofLactobacillus pontis and Two Related Species in a Sourdough Fermentation , 2000, Applied and Environmental Microbiology.

[149]  J. Songer Clostridial enteric diseases of domestic animals , 1996, Clinical microbiology reviews.

[150]  K. Harmon,et al.  Differentiation of Campylobacter jejuni and Campylobacter coli by polymerase chain reaction. , 1997, Molecular and cellular probes.

[151]  D. Deere,et al.  Survival of cells and DNA of Aeromonas salmonicida released into aquatic microcosms. , 1996, The Journal of applied bacteriology.

[152]  A. Wilcks,et al.  Isolation and characterization of Bacilluscereus-like bacteria from faecal samples from greenhouse workers who are using Bacillus thuringiensis-based insecticides , 2002, International archives of occupational and environmental health.

[153]  J. Songer,et al.  Multiplex polymerase chain reaction assay for genotyping Clostridium perfringens. , 1997, American journal of veterinary research.

[154]  James M. Jay,et al.  Modern food microbiology , 1970 .

[155]  L. Petit,et al.  Clostridium perfringens: toxinotype and genotype. , 1999, Trends in microbiology.

[156]  P. L. Manachini,et al.  Identification of Pediococcus acidilactici and Pediococcus pentosaceus based on 16S rRNA and ldhD gene-targeted multiplex PCR analysis. , 1997, FEMS microbiology letters.

[157]  G. Criseo,et al.  Differentiation of aflatoxin‐producing and non‐producing strains of Aspergillus flavus group , 2001, Letters in applied microbiology.

[158]  E. Borch,et al.  Bacterial spoilage of meat and cured meat products. , 1996, International journal of food microbiology.

[159]  U. Mukhopadhyay,et al.  Novel multiplex PCR approaches for the simultaneous detection of human pathogens: Escherichia coli 0157:H7 and Listeria monocytogenes. , 2007, Journal of microbiological methods.

[160]  G. Anderson,et al.  Multiplex polymerase chain reaction as a mastitis screening test for Staphylococcus aureus, Streptococcus agalactiae, Streptococcus dysgalactiae and Streptococcus uberis in bulk milk samples , 2003, Journal of Dairy Research.

[161]  T. Koivula,et al.  A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. , 1991, Pediatrics.

[162]  A. Holck,et al.  High levels of background flora inhibits growth of Escherichia coli O157:H7 in ground beef. , 2000, International journal of food microbiology.

[163]  John P. Rheeder,et al.  Production of Fumonisin Analogs by Fusarium Species , 2002, Applied and Environmental Microbiology.

[164]  E. Rice,et al.  Isolation of Arcobacter butzleri from ground water , 1999, Letters in applied microbiology.

[165]  K. Ali,et al.  Development of an ultra rapid and simple multiplex polymerase chain reaction technique for detection of Salmonella typhi. , 2006, Saudi medical journal.

[166]  G. Suzzi,et al.  Rapid identification and differentiation of Saccharomyces cerevisiae, Saccharomyces bayanus and their hybrids by multiplex PCR , 2004, Letters in applied microbiology.

[167]  S. Al Dahouk,et al.  Detection of Chromobacterium violaceum by multiplex PCR targeting the prgI, spaO, invG, and sipB genes. , 2006, Systematic and applied microbiology.

[168]  D. L. Harris,et al.  Multiplex PCR assay for detection of Clostridium perfringens in feces and intestinal contents of pigs and in swine feed. , 1998, Veterinary microbiology.

[169]  M. Okabe,et al.  Listeria monocytogenes‐infected bone marrow myeloid cells promote bacterial invasion of the central nervous system , 2004, Cellular microbiology.

[170]  N. Paster,et al.  Detection of aflatoxigenic molds in grains by PCR , 1996, Applied and environmental microbiology.

[171]  M. Slavik,et al.  Development of a triplex PCR assay for the specific detection of Campylobacter jejuni, Salmonella spp., and Escherichia coli O157:H7. , 2003, Molecular and cellular probes.

[172]  O. Kandler Gunus Lactobacillus Beijerinck 1901 , 1986 .

[173]  A. Pizzirani-Kleiner,et al.  PCR method for the detection of potential ochratoxin-producing Aspergillus species in coffee beans. , 2006, Research in microbiology.

[174]  M Wiedmann,et al.  Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential , 1997, Infection and immunity.

[175]  Seonghan Kim,et al.  A Multiplex PCR based Method for the Identification of common Clinical Serotypes of Salmonella enterica subspecies enterica , 2006 .

[176]  L. Villa-Tanaca,et al.  Identification of Candida spp. by Randomly Amplified Polymorphic DNA Analysis and Differentiation between Candida albicans and Candida dubliniensis by Direct PCR Methods , 2003, Journal of Clinical Microbiology.

[177]  S. Monday,et al.  Use of Multiplex PCR To Detect Classical and Newly Described Pyrogenic Toxin Genes in Staphylococcal Isolates , 1999, Journal of Clinical Microbiology.

[178]  K. L. Hopkins,et al.  Simultaneous molecular subtyping and shiga toxin gene detection in Escherichia coli using multiplex polymerase chain reaction , 2000, Letters in applied microbiology.

[179]  P. Fratamico,et al.  A multiplex polymerase chain reaction for the differentiation of Campylobacter jejuni and Campylobacter coli from a swine processing facility and characterization of isolates by pulsed-field gel electrophoresis and antibiotic resistance profiles. , 2002, Journal of food protection.

[180]  Ana Tereza Ribeiro de Vasconcelos,et al.  The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[181]  R. Yolken,et al.  Effect of long term consumption of infant formulas with bifidobacteria (B) and s. thermophilus (ST) on stool patterns and diaper rash in infants , 1998 .

[182]  O. Erkmen Behavior of Staphylococcus aureus in refrigerated and frozen ground beef and in Turkish style sausage and broth with and without additives , 1997 .

[183]  S. Altekruse,et al.  Campylobacter jejuni--an emerging foodborne pathogen. , 1999, Emerging infectious diseases.

[184]  Emilio Bouza,et al.  Evaluation of a New System, VITEK 2, for Identification and Antimicrobial Susceptibility Testing of Enterococci , 2000, Journal of Clinical Microbiology.

[185]  M. Blaser,et al.  Campylobacter Jejuni: Current Status and Future Trends , 1992 .

[186]  J. D. Elsas,et al.  Molecular Microbial Ecology Manual , 2013, Springer Netherlands.

[187]  G. Fitzgerald,et al.  A rapid PCR based method to distinguish between Lactococcus and Enterococcus. , 2000, Systematic and applied microbiology.

[188]  H. Claus,et al.  vanA-mediated high-level glycopeptide resistance in Enterococcus faecium from animal husbandry. , 1995, FEMS microbiology letters.

[189]  K. Omoe,et al.  Detection of seg, seh, and sei genes in Staphylococcus aureus Isolates and Determination of the Enterotoxin Productivities of S. aureus Isolates Harboring seg, seh, or sei Genes , 2002, Journal of Clinical Microbiology.

[190]  G. Fleet Wine Microbiology and Biotechnology , 1993 .

[191]  Gehua Wang,et al.  Multiplex PCR for Detection of Genes forStaphylococcus aureus Enterotoxins, Exfoliative Toxins, Toxic Shock Syndrome Toxin 1, and Methicillin Resistance , 2000, Journal of Clinical Microbiology.

[192]  B. Goldin,et al.  Probiotics for humans , 1992 .

[193]  A. Querol,et al.  A new PCR-based method for monitoring inoculated wine fermentations. , 2003, International journal of food microbiology.

[194]  D. Zarlenga,et al.  PCR as a diagnostic and quantitative technique in veterinary parasitology. , 2001, Veterinary parasitology.

[195]  H. Abriouel,et al.  Isolation of bacteriocinogenic Lactobacillus plantarum strains from ben saalga, a traditional fermented gruel from Burkina Faso. , 2006, International journal of food microbiology.

[196]  L. E. Jeremiah,et al.  Bacterial mediated off-flavours in retail-ready beef after storage in controlled atmospheres , 2000 .

[197]  K. Eisenach,et al.  Quantitative Analysis of mRNA as a Marker for Viability of Mycobacterium tuberculosis , 1999, Journal of Clinical Microbiology.

[198]  M. Sydney,et al.  Campylobacter upsaliensis: Another Pathogen for Consideration in the United States , 2002 .

[199]  B. Swaminathan,et al.  PulseNet standardized protocol for subtyping Listeria monocytogenes by macrorestriction and pulsed-field gel electrophoresis. , 2001, International journal of food microbiology.

[200]  I. Wesley,et al.  Infection of cesarean-derived colostrum-deprived 1-day-old piglets with Arcobacter butzleri, Arcobacter cryaerophilus, and Arcobacter skirrowii , 1996, Infection and immunity.

[201]  W. Holzapfel,et al.  Enterococci at the crossroads of food safety? , 1999, International journal of food microbiology.

[202]  F M Aarestrup,et al.  Occurrence of glycopeptide resistance among Enterococcus faecium isolates from conventional and ecological poultry farms. , 1995, Microbial drug resistance.

[203]  A. Stacey,et al.  Isolation of Arcobacter butzleri from a neonate with bacteraemia. , 1995, The Journal of infection.

[204]  A. Hightower,et al.  Epidemic listeriosis--evidence for transmission by food. , 1983, The New England journal of medicine.

[205]  R. Brosch,et al.  Genomic fingerprinting of 80 strains from the WHO multicenter international typing study of listeria monocytogenes via pulsed-field gel electrophoresis (PFGE). , 1996, International journal of food microbiology.

[206]  P. Hamal,et al.  Primer R108 performs best in the RAPD strain typing of threeAspergillus species frequently isolated from patients , 2008, Folia Microbiologica (Prague).

[207]  L. Herman,et al.  Detection and characterization of verotoxigenic Escherichia coli by a VTEC/EHEC multiplex PCR in porcine faeces and pig carcass swabs. , 2003, Research in microbiology.

[208]  A. Schuchat,et al.  Reduction in the incidence of human listeriosis in the United States. Effectiveness of prevention efforts? The Listeriosis Study Group. , 1995, JAMA.

[209]  B K Simpson,et al.  Aflatoxins in food: occurrence, biosynthesis, effects on organisms, detection, and methods of control. , 1991, Critical reviews in food science and nutrition.

[210]  C. R. McClung,et al.  Campylobacter nitrofigilis sp. nov., a Nitrogen-Fixing Bacterium Associated with Roots of Spartina alterniflora Loisel , 1983 .

[211]  B. Swaminathan,et al.  Restriction fragment length polymorphisms in the ribosomal genes for species identification and subtyping of aerotolerant Campylobacter species , 1991, Journal of clinical microbiology.

[212]  R. Whiley,et al.  The genus Streptococcus , 1995 .

[213]  in chief George M. Garrity Bergey’s Manual® of Systematic Bacteriology , 1989, Springer New York.

[214]  H. Seeliger,et al.  Chapter II Serotyping of Listeria monocytogenes and Related Species , 1979 .

[215]  R. Odedra,et al.  Multiplex PCRs for Identification of Escherichia coliVirulence Genes , 2000, Journal of Clinical Microbiology.

[216]  W. Holzapfel,et al.  The Genera of Lactic Acid Bacteria , 1999 .

[217]  E. H. Marth,et al.  Listeria, Listeriosis, and Food Safety, Third Edition , 2007 .

[218]  L. Domínguez,et al.  Unusual Outbreak of Clinical Mastitis in Dairy Sheep Caused by Streptococcus equi subsp. zooepidemicus , 2002, Journal of Clinical Microbiology.

[219]  S. Altekruse,et al.  Emerging foodborne diseases. , 1997, Emerging infectious diseases.