Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA)

Van Belkum, Alex

doi:10.1111/j.1574-695x.2006.00173.x

Cited by 203Bacterial Identification and Susceptibility TestingAntimicrobial Resistance in StaphylococcusGenetic diversity and population structure

Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA)

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Van Belkum, Alex·2007·FEMS Immunology & Medical Microbiology

DOI 10.1111/j.1574-695x.2006.00173.x

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Abstract

All bacterial genomes contain multiple loci of repetitive DNA. Repeat unit sizes and repeat sequences may vary when multiple loci are considered for different isolates of an individual microbial species. Moreover, it has been documented on many occasions that the number of repeat units per locus is a strain-defining parameter. Consequently, there is isolate-specificity in the number of repeats per locus when different strains of a given bacterial species are compared. The experimental assessment of this variability for a number of different loci has been called 'multilocus variable number of tandem repeat analysis' (MLVA). The approach can be supported or extended by locus-specific DNA sequencing for establishing mutations in the individual repeat units, which usually enhances the resolution of the approach considerably. Essentially, MLVA with or without supportive sequencing has been developed for all of the medically relevant bacterial species and can be used effectively for tracing outbreaks or other forms of bacterial dissemination. MLVA is a modern, timely and versatile bacterial typing methodology.

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Distributions of TRs in genomic loci are recognized as the variable number of TR regions widely used to determine inherited traits and for molecular typing in prokaryotic and eukaryotic species.
“Distributions of TRs in the genomic loci are also recognized as the variable number of TR regions that have been widely used to determine an individual's inherited traits as well as for molecular typing both in prokaryotic and eukaryotic species.61”
From Whole genomic DNA sequencing and comparative genomic analysis ofArthrospira platensis: high genome plasticity and genetic diversity (2016) · cites this paper as [61]
The Introduction defines variable-number tandem-repeat regions (VNTRs), says they occur in essentially all prokaryotic and eukaryotic species, and reports their use for identification. The section on technological improvements also describes human genotyping and forensic DNA fingerprinting. Neither passage says VNTRs are used to determine an individual's inherited traits. (LLM, conf=0.86)
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MethodSelf-citation
Disease interaction and pathogens exchange between wild and farmed fish populations with special reference to Norway
Johansen, L., Jensen, I., Mikkelsen, H., Bjørn, P.-A., Jansen, P. A., & Bergh, Ø. (2011) · Aquaculture · doi:10.1016/j.aquaculture.2011.02.014 · Cited by 196 · see citing works
Phylogenetics of a Fungal Invasion: Origins and Widespread Dispersal of White-Nose Syndrome
Drees, K. P., Lorch, J. M., Puechmaille, S. J., Parise, K. L., Wibbelt, G., Hoyt, J. R., Sun, K., Jargalsaikhan, A., Dalannast, M., Palmer, J. M., et al. (2017) · mBio · doi:10.1128/mbio.01941-17 · Cited by 118 · see citing works
Recommended minimal standards for description of new taxa of the genera Bifidobacterium, Lactobacillus and related genera
Mattarelli, P., Holzapfel, W. H., Franz, C. M. A. P., Endo, A., Felis, G. E., Hammes, W. P., Pot, B., Dicks, L. M. T., & Dellaglio, F. (2014) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.060046-0 · Cited by 104 · see citing works
Single-Nucleotide-Polymorphism Genotyping ofCoxiella burnetiiduring a Q Fever Outbreak in The Netherlands
Huijsmans, C. J. J., Schellekens, J. J. A., Wever, P. C., Toman, R., Savelkoul, P. H. M., Janse, I., & Hermans, M. H. A. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02293-10 · Cited by 90 · see citing works
Nonculture Molecular Techniques for Diagnosis of Bacterial Disease in Animals
Cai, H. Y., Caswell, J., & Prescott, J. F. (2014) · Veterinary Pathology · doi:10.1177/0300985813511132 · Cited by 84 · see citing works
“reactions for specific bacterial species and may generate artifacts in typing profiles because of PCR inaccuracy.(66) As the cost of high-throughput DNA sequencing becomes ever lower, comparing the genomes of bacterial isolates may be done for routine diagnosis in the near future.”
Background
Epidemic Genotype ofCoxiella burnetiiamong Goats, Sheep, and Humans in the Netherlands
Tilburg, J. J. H. C., Roest, H.-J., Buffet, S., Nabuurs-Franssen, M. H., Horrevorts, A. M., Raoult, D., & Klaassen, C. H. W. (2012) · Emerging infectious diseases · doi:10.3201/eid1805.111907 · Cited by 80 · see citing works
Evaluation of the DiversiLab System for Detection of Hospital Outbreaks of Infections by Different Bacterial Species
Fluit, A. C., Terlingen, A. M., Andriessen, L., Ikawaty, R., van Mansfeld, R., Top, J., Stuart, J. W. C., Hall, M. A. L., & Boel, C. H. E. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.01191-10 · Cited by 78 · see citing works
Identification of Variable-Number Tandem-Repeat (VNTR) Sequences in Acinetobacter baumannii and Interlaboratory Validation of an Optimized Multiple-Locus VNTR Analysis Typing Scheme
Pourcel, C., Minandri, F., Hauck, Y., D’Arezzo, S., Imperi, F., Vergnaud, G., & Visca, P. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.02003-10 · Cited by 75 · see citing works
spa Typing for Epidemiological Surveillance of Staphylococcus aureus
Hallin, M., Friedrich, A. W., & Struelens, M. J. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-999-4_15 · Cited by 74 · see citing works
Practical relevance of methodologies for detecting and tracing of Listeria monocytogenes in ready-to-eat foods and manufacture environments – A review
Žunabović-Pichler, M., Domig, K. J., & Kneifel, W. (2010) · LWT · doi:10.1016/j.lwt.2010.08.005 · Cited by 70 · see citing works
Multiple-locus variable-number tandem-repeats analysis of Listeria monocytogenes using multicolour capillary electrophoresis and comparison with pulsed-field gel electrophoresis typing
Lindstedt, B.-A., Tham, W., Danielsson‐Tham, M., Vardund, T., Helmersson, S., & Kapperud, G. (2007) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2007.11.012 · Cited by 68 · see citing works
Phylogeography and population structure of the biologically invasive phytopathogen E rwinia amylovora inferred using minisatellites
Bühlmann, A., Dreo, T., Rezzonico, F., Pothier, J. F., Smits, T. H. M., Ravnikar, M., Frey, J. E., & Duffy, B. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12289 · Cited by 66 · see citing works
Bacteriological diagnosis and molecular strain typing of Mycobacterium bovis and Mycobacterium caprae
Gormley, E. P., Corner, L. A. L., Costello, E., & Rodríguez, S. (2014) · Research in Veterinary Science · doi:10.1016/j.rvsc.2014.04.010 · Cited by 63 · see citing works
Multiple-Locus Variable-Number Tandem-Repeat Assay Analysis of Methicillin-ResistantStaphylococcus aureusStrains
Tenover, F. C., Vaughn, R. R., McDougal, L. K., Fosheim, G. E., & McGowan, J. E. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.02451-06 · Cited by 63 · see citing works
“The ability to type MRSA strains rapidly in clinical microbiology laboratories and to differentiate between the multiresistant MRSA strains associated with health care facilities and the more susceptible community-associated MRSA strains could improve public health and infection control efforts to reduce MRSA spread i…”
Background
Acquisition and Cross-Transmission of Staphylococcus aureus in European Intensive Care Units
Bloemendaal, A. L. A., Fluit, A. C., Jansen, W. T. M., Vriens, M. R., Ferry, T., Argaud, L., Amorim, J. M., Resende, A. C., Pascual, Á., López‐Cerero, L., et al. (2009) · Infection Control and Hospital Epidemiology · doi:10.1086/593126 · Cited by 60 · see citing works
Advances in typing and identification of foodborne pathogens
Wei, X., & Zhao, X. (2020) · Current Opinion in Food Science · doi:10.1016/j.cofs.2020.09.002 · Cited by 55 · see citing works
Bacterial Strain Typing
MacCannell, D. (2013) · Clinics in Laboratory Medicine · doi:10.1016/j.cll.2013.03.005 · Cited by 55 · see citing works
Multilocus Variable-Number Tandem-Repeat Analysis of Mycoplasma pneumoniae Clinical Isolates from 1962 to the Present: a Retrospective Study
Benitez, A. J., Diaz, M. H., Wolff, B. J., Pimentel, G., Njenga, M. K., Estévez, A., & Winchell, J. M. (2012) · Journal of Clinical Microbiology · doi:10.1128/jcm.01755-12 · Cited by 54 · see citing works
Culture-independent multi-locus variable-number tandem-repeat analysis (MLVA) of Mycoplasma pneumoniae
Dumke, R., & Jacobs, E. (2011) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2011.06.008 · Cited by 54 · see citing works
ALegionella pneumophilacollagen-like protein encoded by a gene with a variable number of tandem repeats is involved in the adherence and invasion of host cells
Vandersmissen, L., Buck, E. D. J. D., Saels, V., Coil, D. A., & Anné, J. (2010) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.01951.x · Cited by 54 · see citing works
“…of multiple genotyping methods for epidemiological studies (Cazalet et al., 2004, 2008; Gaia et al., 2005; Pourcel et al., 2007), and variable number of tandem repeats (VNTRs) analysis is one of the methods used for the classification of outbreaks of infectious diseases (van Belkum, 2007).”
Method
Molecular‐based identification and detection ofSalmonellain food production systems: current perspectives
Ricke, S. C., Kim, S. A., Shi, Z., & Park, S. H. (2018) · Journal of Applied Microbiology · doi:10.1111/jam.13888 · Cited by 57 · see citing works
“…MLST to be combined with other methods, such as VNTR (variable number tandem repeats), designated MLVA (multilocus variable number of tandem repeats analysis), to increase the resolution of closely related Salmonella isolates (Foley et al. 2006; Van Belkum 2007; Ricke et al. 2015; Fu et al. 2016).”
Method
Trends in Molecular Diagnosis and Diversity Studies for Phytosanitary Regulated Xanthomonas
Catara, V., Cubero, J., Pothier, J. F., Bosis, E., Bragard, C., Đermić, E., Holeva, M. C., Jacques, M., Petter, F., Pruvost, O., et al. (2021) · Microorganisms · doi:10.3390/microorganisms9040862 · Cited by 53 · see citing works
An overview of various typing methods for clinical epidemiology of the emerging pathogen Stenotrophomonas maltophilia
Gherardi, G., Creti, R., Pompilio, A., & Bonaventura, G. D. (2014) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2014.11.005 · Cited by 52 · see citing works
Controlled Performance Evaluation of the DiversiLab Repetitive-Sequence-Based Genotyping System for Typing Multidrug-Resistant Health Care-Associated Bacterial Pathogens
Deplano, A., Denis, O., Rodriguez‐Villalobos, H., Ryck, R. D., Struelens, M. J., & Hallin, M. (2011) · Journal of Clinical Microbiology · doi:10.1128/jcm.00528-11 · Cited by 51 · see citing works
Listeria monocytogenes in foods—From culture identification to whole‐genome characteristics
Osek, J., Lachtara, B., & Wieczorek, K. (2022) · Food Science & Nutrition · doi:10.1002/fsn3.2910 · Cited by 49 · see citing works
Genomic Survey of Pathogenicity Determinants and VNTR Markers in the Cassava Bacterial Pathogen Xanthomonas axonopodis pv. Manihotis Strain CIO151
Arrieta‐Ortiz, M. L., Rodriguez‐R, L. M., Pérez‐Quintero, Á. L., Poulin, L., Díaz, A. C., Rojas, N. A., Trujillo, C., Benavides, M. R., Bart, R. S., Boch, J., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079704 · Cited by 49 · see citing works
Selection and Validation of a Multilocus Variable-Number Tandem-Repeat Analysis Panel for Typing Shigella spp
Gorgé, O., Lopez, S., Hilaire, V., Lisanti, O., Ramisse, V., & Vergnaud, G. (2008) · Journal of Clinical Microbiology · doi:10.1128/jcm.02027-07 · Cited by 47 · see citing works
Structures and stability of simple DNA repeats from bacteria
Brázda, V., Fojta, M., & Bowater, R. P. (2020) · Biochemical Journal · doi:10.1042/bcj20190703 · Cited by 47 · see citing works
New system for multilocus variable‐number tandem‐repeat analysis of the enterohemorrhagic Escherichia coli strains belonging to three major serogroups: O157, O26, and O111
Izumiya, H., Pei, Y., Terajima, J., Ohnishi, M., Hayashi, T., Iyoda, S., & Watanabe, H. (2010) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2010.00252.x · Cited by 47 · see citing works
Improving resolution of public health surveillance for human Salmonella entericaserovar Typhimurium infection: 3 years of prospective multiple-locus variable-number tandem-repeat analysis (MLVA)
Sintchenko, V., Wang, Q., Howard, P., Ha, C. W. Y., Kardamanidis, K., Musto, J., & Gilbert, G. L. (2012) · BMC Infectious Diseases · doi:10.1186/1471-2334-12-78 · Cited by 46 · see citing works
Impact of Strain Typing Methods on Assessment of Relationship between Paired Nares and Wound Isolates of Methicillin-Resistant Staphylococcus aureus
Clarridge, J. E., Harrington, A., Roberts, M. C., Soge, O. O., & Maquelin, K. (2012) · Journal of Clinical Microbiology · doi:10.1128/jcm.02423-12 · Cited by 44 · see citing works
Feral swine brucellosis in the United States and prospective genomic techniques for disease epidemiology
Leiser, O. P., Corn, J. L., Schmit, B. S., Keim, P., & Foster, J. T. (2013) · Veterinary Microbiology · doi:10.1016/j.vetmic.2013.02.025 · Cited by 43 · see citing works
Genotyping to distinguish microbial pathogenicity in periodontitis
Kuboniwa, M., Inaba, H., & Amano, A. (2010) · Periodontology 2000 · doi:10.1111/j.1600-0757.2010.00352.x · Cited by 42 · see citing works
Development of variable number of tandem repeats typing schemes for Ralstonia solanacearum, the agent of bacterial wilt, banana Moko disease and potato brown rot
N’Guessan, C. A., Brisse, S., Roux, A.-C. L., Poussier, S., Koné, D., & Wicker, E. (2013) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2013.01.012 · Cited by 42 · see citing works
Development of a Variable Number of Tandem Repeats Typing Scheme for the Bacterial Rice Pathogen Xanthomonas oryzae pv. oryzicola
Zhao, S., Poulin, L., Rodriguez‐R, L. M., Serna, N. F., Liu, S., Wonni, I., Szurek, B., Verdier, V., Leach, J. E., He, Y.-Q., et al. (2012) · Phytopathology · doi:10.1094/phyto-04-12-0078-r · Cited by 41 · see citing works
Molecular analysis of Coxiella burnetii in Germany reveals evolution of unique clonal clusters
Frangoulidis, D., Walter, M. C., Antwerpen, M. H., Zimmermann, P., Janowetz, B., Alex, M., Böttcher, J., Henning, K., Hilbert, A., Ganter, M., et al. (2014) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2014.06.011 · Cited by 41 · see citing works
RAPD and VNTR analyses demonstrate genotypic heterogeneity of Mycoplasma hyopneumoniae isolates from pigs housed in a region with high pig density
Nathues, H., Beilage, E. G., Kreienbrock, L., Rosengarten, R., & Spergser, J. (2011) · Veterinary Microbiology · doi:10.1016/j.vetmic.2011.05.029 · Cited by 41 · see citing works
High-throughput typing of Staphylococcus aureus by amplified fragment length polymorphism (AFLP) or multi-locus variable number of tandem repeat analysis (MLVA) reveals consistent strain relatedness
Melles∗, D. C., Schouls, L. M., François, P., Herzig, S., Verbrugh, H. A., van Belkum, A., & Schrenzel, J. (2008) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-008-0585-4 · Cited by 41 · see citing works
Multilocus Variable-Number-Tandem-Repeats Analysis (MLVA) distinguishes a clonal complex of Clavibacter michiganensis subsp. michiganensis strains isolated from recent outbreaks of bacterial wilt and canker in Belgium
Załuga, J., Stragier, P., Vaerenbergh, J. V., Maes, M., & Vos, P. D. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-126 · Cited by 40 · see citing works
Whole genomic DNA sequencing and comparative genomic analysis ofArthrospira platensis: high genome plasticity and genetic diversity
Xu, T., Qin, S., Hu, Y., Song, Z., Ying, J., Li, P., Dong, W., Zhao, F., Yang, H., & Bao, Q. (2016) · DNA Research · doi:10.1093/dnares/dsw023 · Cited by 37 · see citing works
“Distributions of TRs in the genomic loci are also recognized as the variable number of TR regions that have been widely used to determine an individual’s inherited traits as well as for molecular typing both in prokaryotic and eukaryotic species.(61) Based on the size of the repeat motif, TRs were classified into micr…”
Background
MLVA-16 loci panel on Brucella spp. using multiplex PCR and multicolor capillary electrophoresis
Garofolo, G., Ancora, M., & Giannatale, E. D. (2012) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2012.11.007 · Cited by 39 · see citing works
Multiple-locus variable-nucleotide tandem repeat subtype analysis implicates European starlings as biological vectors for Escherichia coli O157:H7 in Ohio, USA
Williams, M. L., Pearl, D. L., & LeJeune, J. T. (2011) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2011.05102.x · Cited by 37 · see citing works
Multi-locus variable number tandem repeat analysis of 7th pandemic Vibrio cholerae
Lam, C., Octavia, S., Reeves, P. R., & Lan, R. (2012) · BMC Microbiology · doi:10.1186/1471-2180-12-82 · Cited by 37 · see citing works
Investigation of Cyprinid herpesvirus-3 genetic diversity by a multi-locus variable number of tandem repeats analysis
Avarre, J., Madeira, J.-P., Santika, A., Zainun, Z., Baud, M., Cabon, J., Caruso, D., Castric, J., Bigarré, L., Engelsma, M. Y., et al. (2011) · Journal of Virological Methods · doi:10.1016/j.jviromet.2011.03.002 · Cited by 35 · see citing works
Regional Profiling for Determination of Genotype Diversity of Mastitis-Specific Staphylococcus aureus Lineage in Canada by Use of Clumping Factor A, Pulsed-Field Gel Electrophoresis, and spa Typing
Said, K. B., Ismaïl, J., Campbell, J., Mulvey, M. R., Bourgault, A., Messier, S. J., & Zhao, X. (2009) · Journal of Clinical Microbiology · doi:10.1128/jcm.01768-09 · Cited by 35 · see citing works
Analysis of Salmonella enterica Serovar Typhimurium Variable-Number Tandem-Repeat Data for Public Health Investigation Based on Measured Mutation Rates and Whole-Genome Sequence Comparisons
Dimovski, K., Cao, H., Wijburg, O. L. C., Strugnell, R. A., Mantena, R. K. R., Whipp, M., Hogg, G. G., & Holt, K. E. (2014) · Journal of Bacteriology · doi:10.1128/jb.01820-14 · Cited by 34 · see citing works
Characterization of Shigella sonnei isolates from travel-associated cases in Japan
Izumiya, H., Tada, Y., Ito, K., Morita‐Ishihara, T., Ohnishi, M., Terajima, J., & Watanabe, H. (2009) · Journal of Medical Microbiology · doi:10.1099/jmm.0.011809-0 · Cited by 33 · see citing works
“1486 011809 G 2009 SGM Printed in Great Britain Downloaded from www.microbiologyresearch.org by IP: 54.70.40.11 On: Wed, 07 Nov 2018 16:58:56 molecular typing method that has been applied to several bacterial pathogens, including S. sonnei (Liang et al., 2007; van Belkum, 2007).”
MethodInfluential
Genotyping of Coxiella burnetii in sheep and goat abortion samples
Chochlakis, D., Santos, A. S., Giadinis, N. D., Papadopoulos, D., Boubaris, L., Kalaitzakis, E., Psaroulaki, A., Kritas, S. K., & Petridou, E. (2018) · BMC Microbiology · doi:10.1186/s12866-018-1353-y · Cited by 33 · see citing works
Genotyping of Leptospira interrogans strains from Argentina by Multiple-Locus Variable-number tandem repeat Analysis (MLVA)
Paván, M. E., Cairó, F., Pettinari, M. J., Samartino, L., & Brihuega, B. F. (2010) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2010.06.002 · Cited by 32 · see citing works
Development of 14 minisatellite markers for the citrus canker bacterium, Xanthomonas citri pv. citri
Ngoc, L. B. T., VERNIERE, C., VITAL, K., Guérin, F., Gagnevin, L., Brisse, S., Ah-You, N., & Pruvost, O. (2008) · Molecular Ecology Resources · doi:10.1111/j.1755-0998.2008.02242.x · Cited by 31 · see citing works
A multiple-locus variable-number tandem repeat analysis (MLVA) ofListeria monocytogenesisolated from Norwegian salmon-processing factories and from listeriosis patients
Lunestad, B. T., TRUONG, T. T. T., & Lindstedt, B.-A. (2012) · Epidemiology and Infection · doi:10.1017/s0950268812002750 · Cited by 30 · see citing works
Genetic diversity of Haemophilus parasuis from sick and healthy pigs
Boerlin, P., Poljak, Z., Gallant, J., Chalmers, G., Nicholson, V. M., Soltes, G. A., & MacInnes, J. I. (2013) · Veterinary Microbiology · doi:10.1016/j.vetmic.2013.07.028 · Cited by 29 · see citing works
Multiple-Locus Variable-Number Tandem-Repeat Analysis in Genotyping Yersinia enterocolitica Strains from Human and Porcine Origins
Virtanen, S., Laukkanen‐Ninios, R., Martínez, P. O., Siitonen, A., Fredriksson‐Ahomaa, M., & Korkeala, H. J. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.00710-13 · Cited by 29 · see citing works
“Different genotypes are distinguished by the number of repeats in each locus (18).”
Background
Development of Multiple-Locus Variable-Number Tandem-Repeat Analysis for the Molecular Subtyping of Enterobacter sakazakii
Mullane, N., Ryan, M. T., Iversen, C., Murphy, M., Gaora, P. Ó., Quinn, T., Whyte, P., Wall, P. G., & Fanning, S. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01726-07 · Cited by 29 · see citing works
Multiple-locus variable-number tandem-repeat analysis (MLVA) genotyping of human Brucella isolates in Malaysia
Tay, B. Y., Ahmad, N., Hashim, R., Zahidi, J. M., Thong, K. L., Koh, X. P., & Noor, A. M. (2015) · BMC Infectious Diseases · doi:10.1186/s12879-015-0958-0 · Cited by 28 · see citing works
Double Trouble: Medical Implications of Genetic Duplication and Amplification in Bacteria
Craven, S. H., & Neidle, E. L. (2007) · Future Microbiology · doi:10.2217/17460913.2.3.309 · Cited by 28 · see citing works
“In some cases, molecular epidemiology is even facilitated by variation in the number of tandem repeats [44,45].”
BackgroundMethod
Novel Multiple-Locus Variable-Number Tandem-Repeat Analysis Method for Rapid Molecular Typing of Human Staphylococcus aureus
Ikawaty, R., Willems, R. J. L., Box, A. T. A., Verhoef, J., & Fluit, A. C. (2008) · Journal of Clinical Microbiology · doi:10.1128/jcm.00861-08 · Cited by 27 · see citing works
A Comprehensive Review of Detection Methods for Staphylococcus aureus and Its Enterotoxins in Food: From Traditional to Emerging Technologies
Mairi, A., Ibrahim, N. A., Idres, T., & Touati, A. (2025) · Toxins · doi:10.3390/toxins17070319 · Cited by 26 · see citing works
Advances in subtyping methods of foodborne disease pathogens
Boxrud, D. J. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.02.011 · Cited by 26 · see citing works
Genetic structure analysis of strains causing citrus canker in I ran reveals the presence of two different lineages of X anthomonas citri pv. citri pathotype A*
Pruvost, O., Goodarzi, T., Boyer, K., Soltaninejad, H., Escalon, A., Alavi, S. M., Javegny, S., Boyer, C., Cottyn, B. G., Gagnevin, L., et al. (2014) · Plant Pathology · doi:10.1111/ppa.12324 · Cited by 26 · see citing works
Examination of clinical and environmental Vibrio parahaemolyticus isolates by multi-locus sequence typing (MLST) and multiple-locus variable-number tandem-repeat analysis (MLVA)
Lüdeke, C. H. M., González‐Escalona, N., Fischer, M. J., & Jones, J. L. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00564 · Cited by 25 · see citing works
“The VNTRs are highly polymorphic and are well suited for differentiation of bacterial isolates (Lindstedt, 2005; van Belkum, 2007).”
Background
Bacillus anthracis and Other Bacillus Species
Cote, C. K., Heffron, J. D., Bozue, J. A., & Welkos, S. L. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397169-2.00102-5 · Cited by 25 · see citing works
Multiple-Locus Variable-Number Tandem-Repeat Analysis of the Swine Dysentery Pathogen, Brachyspira hyodysenteriae
Hidalgo, Á., Carvajal, A., La, T., Naharro, G., Rubio, P., Phillips, N. D., & Hampson, D. J. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.00348-10 · Cited by 25 · see citing works
Strain Typing Using Multiple “Variable Number of Tandem Repeat” Analysis and Genetic Element CRISPR
Pourcel, C., & Vergnaud, G. (2011) · Molecular Microbiology · doi:10.1128/9781555816834.ch11 · Cited by 24 · see citing works
Phylogenetic Analysis of EnterohemorrhagicEscherichia coliO157, Germany, 1987–2008
Jenke, C., Harmsen, D., Weniger, T., Rothgänger, J., Hyytia-Trees, E. K., Bielaszewska, M., Karch, H., & Mellmann, A. (2010) · Emerging infectious diseases · doi:10.3201/eid1604.091361 · Cited by 23 · see citing works
Overview of Molecular Typing Tools for The Characterization of Salmonella enterica in Malaysia.
Ngoi, S. T., Teh, C. S. J., Chai, L. C., & Thong, K. L. (2015) · PubMed · doi:10.3967/bes2015.105 · Cited by 23 · see citing works
Evaluation of MLVA for epidemiological typing and outbreak detection of ESBL-producing Escherichia coli in Sweden
Helldal, L., Karami, N., Welinder‐Olsson, C., Moore, E. R. B., & Åhrén, C. (2017) · BMC Microbiology · doi:10.1186/s12866-016-0922-1 · Cited by 23 · see citing works
Evaluation of a highly discriminating multiplex multi-locus variable-number of tandem-repeats (MLVA) analysis for Vibrio cholerae
Olsen, J. S., Aarskaug, T., Skogan, G., Fykse, E. M., Ellingsen, A. B., & Blatny, J. M. (2009) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2009.06.011 · Cited by 23 · see citing works
PCR-based rapid genotyping of Stenotrophomonas maltophiliaisolates
Roscetto, E., Rocco, F., Carlomagno, M. S., Casalino, M., Colonna, B., Zarrilli, R., & Nocera, P. P. D. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-202 · Cited by 23 · see citing works
Molecular and genotyping techniques in diagnosis of Coxiella burnetii: An overview
Khademi, P., Tukmechi, A., Sgroi, G., Ownagh, A., Enferadi, A., Khalili, M., & Mardani, K. (2024) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2024.105655 · Cited by 22 · see citing works
Multiple-Locus Variable-Number Tandem Repeat Analysis ofVibrio choleraein Comparison with Pulsed Field Gel Electrophoresis and Virulotyping
Teh, C. S. J., Chua, K. H., & Thong, K. L. (2010) · BioMed Research International · doi:10.1155/2010/817190 · Cited by 22 · see citing works
Insertion Sequence- and Tandem Repeat-Based Genotyping Techniques for Xanthomonas citri pv. mangiferaeindicae
Pruvost, O., Vernière, C., Vital, K., Guérin, F., Jouen, E., Chiroleu, F., Ah-You, N., & Gagnevin, L. (2011) · Phytopathology · doi:10.1094/phyto-11-10-0304 · Cited by 22 · see citing works
“15 tandem repeat units per locus is a highly robust strain-defining parameter (48).”
BackgroundInfluential
Multiple-locus, variable number of tandem repeat analysis (MLVA) of the fish-pathogen Francisella noatunensis
Brevik, Ø. J., Ottem, K. F., & Nylund, A. (2011) · BMC Veterinary Research · doi:10.1186/1746-6148-7-5 · Cited by 22 · see citing works
Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of Xanthomonas citri pv. citri at microgeographic scales in a tropical area of Asiatic citrus canker endemicity
Pruvost, O., Boyer, K., Ravigné, V., Richard, D., & Vernière, C. (2019) · Evolutionary Applications · doi:10.1111/eva.12788 · Cited by 22 · see citing works
“In contrast, MultiLocus Variable number of tandem repeat Analysis (MLVA) has been shown to allow revealing infraspecific genetic diversity in several human monomorphic pathogens (Van Belkum, 2007; Lindstedt, 2005; Pourcel & Vergnaud, 2011).”
Background
Molecular typing of Mycoplasma agalactiae: Tracing European-wide genetic diversity and an endemic clonal population
Nouvel, L., Marenda, M. S., Glew, M. D., Sagné, E., Giammarinaro, P., Tardy, F., Poumarat, F., Rosengarten, R., & Citti, C. (2012) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2012.04.005 · Cited by 21 · see citing works
Population typing of the causal agent of cassava bacterial blight in the Eastern Plains of Colombia using two types of molecular markers
Trujillo, C., Rojas, N. A., Poulin, L., Medina, C. A., Tapiero, A., Restrepo, S., Koebnik, R., & Bernal, A. (2014) · BMC Microbiology · doi:10.1186/1471-2180-14-161 · Cited by 19 · see citing works
Multilocus variable-number of tandem-repeats analysis of Salmonella enterica serotype Gallinarum and comparison with pulsed-field gel electrophoresis genotyping
Bergamini, F., Iori, A., Massi, P., & Pongolini, S. (2010) · Veterinary Microbiology · doi:10.1016/j.vetmic.2010.12.002 · Cited by 19 · see citing works
Genetic diversity of Coxiella burnetii in domestic ruminants in central Italy
Domenico, M. D., Curini, V., Lollo, V. D., Massimini, M., Gialleonardo, L. D., Franco, A., Caprioli, A., Battisti, A., & Cammà, C. (2018) · BMC Veterinary Research · doi:10.1186/s12917-018-1499-8 · Cited by 19 · see citing works
“Since their rapid evolution VNTR are extremely polymorphic, therefore MLVA usually provide a better discriminatory power, which is often suitable for epidemiological purposes [17].”
Background
MLVA and Phage Typing as Complementary Tools in the Epidemiological Investigation of Salmonella enterica serovar Typhimurium Clusters
Ross, I. L., Davos, D. E., Mwanri, L., Raupach, J. C. A., & Heuzenroeder, M. W. (2010) · Current Microbiology · doi:10.1007/s00284-010-9820-1 · Cited by 18 · see citing works
“Discrimination between isolates is based on loci distributed throughout the bacterial genome harboring variable numbers of short repetitive DNA sequences (tandem repeats) [21].”
Background
Molecular Characterization of Salmonella Enteritidis: Comparison of an Optimized Multi-Locus Variable-Number of Tandem Repeat Analysis (MLVA) and Pulsed-Field Gel Electrophoresis
Dewaele, I., Rasschaert, G., Bertrand, S., Wildemauwe, C., Wattiau, P., Imberechts, H., Herman, L., Ducatelle, R., Reu, K. D., & Heyndrickx, M. (2012) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2012.1199 · Cited by 18 · see citing works
“More recently, multilocus variable number of tandem repeat analysis (MLVA) involving ampliﬁcation and fragment size analysis of the number of repeats in the variable number tandem repeat (VNTR) regions has been documented (Van Belkum, 2007).”
Biological Warfare: Infectious Disease and Bioterrorism
Clark, D. P., & Pazdernik, N. J. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-385015-7.00022-3 · Cited by 18 · see citing works
Multiple-locus variable-number tandem repeat analysis of Legionella pneumophila using multi-colored capillary electrophoresis
Nederbragt, A. J., Balasingham, A., Sirevåg, R., Utkilen, H., Jakobsen, K. S., & Anderson-Glenna, M. J. (2008) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2008.02.007 · Cited by 17 · see citing works
Molecular characterization showed limited genetic diversity among Salmonella Enteritidis isolated from humans and animals in Malaysia
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New Multilocus Variable-Number Tandem-Repeat Analysis (MLVA) Scheme for Fine-Scale Monitoring and Microevolution-Related Study of Ralstonia pseudosolanacearum Phylotype I Populations
Guinard, J., Latreille, A., Guérin, F., Poussier, S., & Wicker, E. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.03095-16 · Cited by 16 · see citing works
A new Multi Locus Variable Number of Tandem Repeat Analysis Scheme for epidemiological surveillance of Xanthomonas vasicola pv. musacearum, the plant pathogen causing bacterial wilt on banana and enset
Nakato, G. V., Rojas, J. L. F., Verniere, C., Blondin, L., Coutinho, T. A., Mahuku, G., & Wicker, E. (2019) · PLoS ONE · doi:10.1371/journal.pone.0215090 · Cited by 16 · see citing works
Development and Validation of a Single-Tube Multiple-Locus Variable Number Tandem Repeat Analysis for Klebsiella pneumoniae
Brink, A. A. T. P., von Wintersdorff, C. J. H., van der Donk, C. F. M., Peeters, A. M. M. W., Beisser, P. S., Stobberingh, E. E., & Wolffs, P. F. G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091209 · Cited by 16 · see citing works
Multiple Locus Variable number of tandem repeat Analysis: A molecular genotyping tool for Paenibacillus larvae
Descamps, T., Smet, L. D., Stragier, P., Vos, P. D., & de Graaf, D. C. (2016) · Microbial Biotechnology · doi:10.1111/1751-7915.12375 · Cited by 16 · see citing works
An Optimized Microsatellite Scheme for Assessing Populations of Xanthomonas phaseoli pv. manihotis
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Staphylococcal Interspersed Repeat Unit Typing of Staphylococcus aureus : Evaluation of a New Multilocus Variable-Number Tandem-Repeat Analysis Typing Method
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Food Safety: What Can We Learn From Genomics?
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Multilocus VNTR analysis-ompA typing of venereal isolates of Chlamydia trachomatis in Japan
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Microevolution of Pandemic Vibrio parahaemolyticus Assessed by the Number of Repeat Units in Short Sequence Tandem Repeat Regions
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Contemporary nucleic acid-based molecular techniques for detection, identification, and characterization of Bifidobacterium
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MLVA-NET – a standardised web database for bacterial genotyping and surveillance
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Multiple‐locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria
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Multiple Locus VNTR (Variable Number of Tandem Repeat) Analysis
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Use of multilocus variable-number tandem repeat analysis (MLVA) in eight European countries, 2012
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MLVA (multi-locus variable-length repeat analysis)
(2008) · Springer eBooks · doi:10.1007/978-1-4020-6754-9_10595

Authors: Van Belkum, A.
Venue: FEMS Immunology & Medical Microbiology
Publisher: Oxford University Press (OUP)
Published: 2007-02
Volume: 49
Issue: 1
Pages: 22-27
ISSN: 0928-8244 (ISSN-L)
1574-695X
DOI: 10.1111/j.1574-695x.2006.00173.x
OpenAlex: W2085293610
Cited by: 203
References: 66
Citations by year: 2026: 1 · 2025: 8 · 2024: 4 · 2022: 3 · 2021: 1 · 2020: 8 · 2019: 9 · 2018: 8 · 2017: 11 · 2016: 11 · 2015: 14 · 2014: 19 · 2013: 18 · 2012: 14
FWCI: 1.43
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: FEMS Immunology & Medical Microbiology (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Bacterial Identification and Susceptibility Testing
Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Keywords: MLVA, strain typing, bacterial genotyping, repetitive DNA, outbreak source tracing, bacterial dissemination
MeSH terms: Bacillus anthracis, Bacteria, DNA, Bacterial, Humans, Mycobacterium tuberculosis, Staphylococcus aureus, Genome, Bacterial, Minisatellite Repeats, Bioterrorism

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Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA)

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