1887

Abstract

is a causal agent of bovine tuberculosis (bTB), one of the most important diseases currently facing the cattle industry worldwide. Tracing the source of infections of livestock is an important tool for understanding the epidemiology of bTB and defining control/eradication strategies. In this study, whole genome sequencing (WGS) of 74 . isolates sourced from naturally infected cattle in the State of Rio Grande do Sul (RS), southern Brazil, was used to evaluate the population structure of in the region, identify potential transmission events and date the introduction of clonal complex (CC) European 2 (Eu2). spoligotyping identified 11 distinct patterns including four new profiles and two CCs, European 1 (Eu1) and Eu2. The analyses revealed a high level of genetic diversity in the majority of herds and identified putative transmission clusters that suggested that within- and between-herd transmission is occurring in RS. In addition, a comparison with other published isolates from Argentina, Brazil, Paraguay and Uruguay demonstrated some evidence for a possible cross-border transmission of CC Eu1 into RS from Uruguay or Argentina. An estimated date for the introduction of CC Eu2 into RS in the middle of the 19th century correlated with the historical introduction of cattle into RS to improve existing local breeds. These findings contribute to the understanding of the population structure of in southern Brazil and highlight the potential of WGS in surveillance and helping to identify bTB transmission.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000569
2021-05-20
2022-01-24
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/5/mgen000569.html?itemId=/content/journal/mgen/10.1099/mgen.0.000569&mimeType=html&fmt=ahah

References

  1. WHO, OIE, FAO, The Union In Roadmap for Zoonotic tuberculosis Geneva: WHO Press; 2017 https://www.oie.int/fileadmin/Home/eng/Our_scientific_expertise/docs/pdf/Tuberculosis/Roadmap_zoonotic_TB.pdf
    [Google Scholar]
  2. OIE In Chapter.3.4.6: Bovine tuberculosis OIE: Terrestrial manual; 2018 https://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/3.04.06_BOVINE_TB.pdf
    [Google Scholar]
  3. Caminiti A. In The Socio-economic Costs of Bovine tuberculosis Bulletin: World Organisation for Animal Health (OIE; 2019 https://oiebulletin.com/index.php?panorama=3-05-tb-costs-en&edition=7591&pdf=panorama&article=8480
    [Google Scholar]
  4. USDA In Livestock and Poultry: World Markets and Trade United States Department of Agriculture, Foreign Agricultural Service; 2020 https://apps.fas.usda.gov/psdonline/circulars/livestock_poultry.pdf
    [Google Scholar]
  5. Secretary of Agricultural Defense, Ministry of Agriculture, Livestock and Supply, Brazil In SDA normative instruction N° 10, March 3, 2017 Brazil: Ministry of Agriculture, Livestock and Supply, Secretary of Agricultural Defense; 2017 pp 1–4 http://www.in.gov.br/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/19124587/do1-2017%E2%80%9306-20-instrucao-normativa-n-10-de-3-de-marco-de-2017%E2%80%9319124353
    [Google Scholar]
  6. Secretariat of Agriculture, Livestock and Agribusiness, Department of Agricultural Defense, State of Rio Grande do Sul, Brazil In Normative Instruction SEAPA 002/2014 Brazil: Secretariat of Agriculture, Livestock and Agribusiness, Department of Agricultural Defense, State of Rio Grande do Sul; 2014 https://www.agricultura.rs.gov.br/upload/arquivos/201611/01155402-pncebt-instrucao-normativa-seapi-002-com-alteracoes.pdf
    [Google Scholar]
  7. Ferreira Neto JS, da Silveira GB, Rosa BM, Gonçalves VSP, Grisi-Filho JHH. Analysis of 15 years of the National program for the control and eradication of animal brucellosis and tuberculosis, Brazil. Semina Ciênc Agrár 2016; 37:3385
    [Google Scholar]
  8. Bahiense L, de Ávila LN, Bavia ME, Amaku M, Dias RA. Prevalence and risk factors for bovine tuberculosis in the state of Bahia, Brazil. Semina Ciênc Agrár 2016; 37:3549
    [Google Scholar]
  9. de Barbieri JM, de Oliveira LF, Dorneles EMS, de Alencar Mota A, Gonçalves VSP. Epidemiological status of bovine tuberculosis in the state of Minas Gerais, Brazil, 2013. Semina Ciênc Agrár 2016; 37:3531–3548
    [Google Scholar]
  10. Dias RA, Ulloa-Stanojlovic FM, Belchior APC, Ferreira RDS, Gonçalves RC. Prevalence and risk factors for bovine tuberculosis in the state of São Paulo, Brazil. Semina Ciênc Agrár 2016; 37:3673
    [Google Scholar]
  11. Galvis JOA, Grisi-Filho JHH, Costa DD, Said A, Amaku M. Epidemiologic characterization of bovine tuberculosis in the state of Espírito Santo, Brazil. Semina Ciênc Agrár 2016; 37:3567
    [Google Scholar]
  12. Guedes IB, Bottene IFN, Monteiro L, Leal Filho JM, Heinemann MB. Prevalence and risk factors for bovine tuberculosis in the state of Mato Grosso do Sul, Brazil. Semina Ciênc Agrár 2016; 37:3579
    [Google Scholar]
  13. Lima PRB, do Nascimento DL, de Almeida EC, Pontual KAQ, Amaku M. Epidemiological situation of bovine tuberculosis in the state of Pernambuco, Brazil. Semina Ciênc Agrár 2016; 37:3601
    [Google Scholar]
  14. Néspoli JMB, Negreiros RL, Amaku M, Dias RA, Ferreira F. Epidemiological situation of bovine tuberculosis in the state of Mato Grosso, Brazil. Semina Ciênc Agrár 2016; 37:3589
    [Google Scholar]
  15. Queiroz MR, Groff ACM, Silva NDS, Grisi-Filho JHH, Amaku M. Epidemiological status of bovine tuberculosis in the state of Rio grande do Sul, Brazil. Semina Ciênc Agrár 2016; 37:3647
    [Google Scholar]
  16. Ribeiro LA, Gonçalves VSP, Francisco PFC, de Alencar Mota ALA, do Nascimento GT et al. Epidemiological status of bovine tuberculosis in the federal district of Brazil. Semina 2016; 37:3561 [View Article]
    [Google Scholar]
  17. Rocha WV, Jayme VDS, de Alencar Mota ALA, de Brito WMED, de Castro Pires GR et al. Prevalence and herd-level risk factors of bovine tuberculosis in the state of Goiás, Brazil. Semina 2016; 37:3625 [View Article]
    [Google Scholar]
  18. Silva MDCP, Gonçalves VSP, de Alencar Mota ALA, Koloda M, Ferreira Neto JS et al. Prevalence and herd-level risk factors for bovine tuberculosis in the state of Paraná, Brazil. Semina 2016; 37:3611 [View Article]
    [Google Scholar]
  19. Veloso FP, Baumgarten KD, de Alencar Mota ALA, Ferreira F, Ferreira Neto JS et al. Prevalence and herd-level risk factors of bovine tuberculosis in the state of SANTA Catarina. Semina 2016; 37:3659 [View Article]
    [Google Scholar]
  20. Vendrame FB, Amaku M, Ferreira F, Telles EO, Grisi-Filho JHH. Epidemiologic characterization of bovine tuberculosis in the state of Rondônia, Brazil. Semina Ciênc Agrár 2016; 37:3639
    [Google Scholar]
  21. ABIEC Beef Report, Brazilian Livestock Profile. ( http://abiec.com.br/en/publicacoes/beef-report-2020-2/) Brazil: Brazilian Beef Exporters Association; 2020
    [Google Scholar]
  22. IBGE IBGE Indicators, Livestock Production Statistics 2019. ( https://biblioteca.ibge.gov.br/visualizacao/periodicos/2380/epp_2019_4tri.pdf) Brazil: Brazilian Institute of Geography and Statistics; 2020
    [Google Scholar]
  23. SEAPDR PNCEBT Statistics in RS: review 2019 ( https://www.agricultura.rs.gov.br/secao-de-vigilancia-zoosanitaria-pncebt) Secretariat of Agriculture, Livestock and Rural Development, Brazil: Porto Alegre; 2020
    [Google Scholar]
  24. Patané JSL, Martins J, Castelão AB, Nishibe C, Montera L. Patterns and processes of Mycobacterium bovis evolution revealed by phylogenomic analyses. Genome Biol Evol 2017; 9:521–535
    [Google Scholar]
  25. Orloski K, Robbe-Austerman S, Stuber T, Hench B, Schoenbaum M. Whole genome sequencing of Mycobacterium bovis isolated from Livestock in the United States, 1989–2018. Front Vet Sci 2018; 5:253
    [Google Scholar]
  26. Crispell J, Cassidy S, Kenny K, McGrath G, Warde S. Mycobacterium bovis genomics reveals transmission of infection between cattle and deer in Ireland. Microb Genomics
    [Google Scholar]
  27. Zimpel CK, Patané JSL, Guedes ACP, de Souza RF, Silva-Pereira TT et al. Global distribution and evolution of Mycobacterium bovis lineages. Front Microbiol 2020; 11:843 [View Article][PubMed]
    [Google Scholar]
  28. Ghavidel M, Mansury D, Nourian K, Ghazvini K. The most common spoligotype of Mycobacterium bovis isolated in the world and the recommended loci for VNTR typing; A systematic review. Microb Pathog 2018; 118:310–315
    [Google Scholar]
  29. Weerasekera D, Pathirane H, Madegedara D, Dissanayake N, Thevanesam V. Evaluation of the 15 and 24-loci MIRU-VNTR genotyping tools with spoligotyping in the identification of Mycobacterium tuberculosis strains and their genetic diversity in molecular epidemiology studies. Infect Dis 2019; 51:206–215
    [Google Scholar]
  30. Carneiro PAM, Pasquatti TN, Takatani H, Zumárraga MJ, Marfil MJ. Molecular characterization of Mycobacterium bovis infection in cattle and buffalo in Amazon Region, Brazil. Vet Med Sci 2020; 6:133–141
    [Google Scholar]
  31. Figueiredo Rocha VC, de Souza-Filho AF, Ikuta CY, Hildebrand E Grisi Filho JH, de Azevedo Issa M et al. High discrimination of Mycobacterium bovis isolates in Brazilian herds by spoligotyping. Prev Vet Med 2020; 179:104976 [View Article][PubMed]
    [Google Scholar]
  32. Trewby H, Wright D, Breadon EL, Lycett SJ, Mallon TR. Use of bacterial whole-genome sequencing to investigate local persistence and spread in bovine tuberculosis. Epidemics 2016; 14:26–35
    [Google Scholar]
  33. Escárcega DAV, Razo CAP, Ruíz SG, Gallegos SLS, Suazo FM. Analysis of bovine tuberculosis transmission in Jalisco, Mexico through whole-genome sequencing. J Vet Res 2020; 64:51–61
    [Google Scholar]
  34. Salvador LCM, O’Brien DJ, Cosgrove MK, Stuber TP, Schooley AM. Disease management at the wildlife‐livestock interface: Using whole‐genome sequencing to study the role of elk in Mycobacterium bovis transmission in Michigan, USA. Mol Ecol 2019; 28:2192–2205
    [Google Scholar]
  35. da Conceição ML, Conceição EC, Furlaneto IP, da Silva SP, dos Santos Guimarães AE. Phylogenomic perspective on a unique Mycobacterium bovis clade dominating bovine tuberculosis infections among cattle and buffalos in Northern Brazil. Sci Rep 1747; 2020:10
    [Google Scholar]
  36. Kao RR, Price-Carter M, Robbe-Austerman S. Use of genomics to track bovine tuberculosis transmission. Rev Sci Tech 2016; 35:241–268
    [Google Scholar]
  37. Biek R, O’Hare A, Wright D, Mallon T, McCormick C. Whole genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badger populations. PLoS Pathog 2012; 8:e1003008
    [Google Scholar]
  38. Ghebremariam MK, Hlokwe T, Rutten V, Allepuz A, Cadmus S. Genetic profiling of Mycobacterium bovis strains from slaughtered cattle in Eritrea. PLoS Negl Trop Dis 2018; 12:e0006406
    [Google Scholar]
  39. Lasserre M, Fresia P, Greif G, Iraola G, Castro-Ramos M. Whole genome sequencing of the monomorphic pathogen Mycobacterium bovis reveals local differentiation of cattle clinical isolates. BMC Genomics 2018; 19:2
    [Google Scholar]
  40. Hauer A, Michelet L, Cochard T, Branger M, Nunez J. Accurate phylogenetic relationships among Mycobacterium bovis strains circulating in France based on whole genome sequencing and single nucleotide polymorphism analysis. Front Microbiol 2019; 10:955
    [Google Scholar]
  41. Zimpel CK, Brandão PE, de Souza Filho AF, de Souza RF, Ikuta CY. Complete genome sequencing of Mycobacterium bovis SP38 and comparative genomics of Mycobacterium bovis and M. tuberculosis strains. Front Microbiol 2017; 8:2389
    [Google Scholar]
  42. Anzai EK. Whole Genome Sequencing of Mycobacterium bovis as an Instrument of Surveillance System in the State of Santa Catarina São Paulo: Faculty of Veterinary Medicine and Animal Science; 2019
    [Google Scholar]
  43. Makovcova J, Babak V, Slany M, Slana I. Comparison of methods for the isolation of mycobacteria from water treatment plant sludge. Antonie van Leeuwenhoek 2015; 107:1165–1179
    [Google Scholar]
  44. Sales ML, Fonseca AA, ÉB S, Cottorello ACP, Issa MA. Evaluation of molecular markers for the diagnosis of Mycobacterium bovis. Folia Microbiol 2014; 59:433–438
    [Google Scholar]
  45. van Embden JDA, van Soolingen D, Small PM, Hermans PWM. Genetic markers for the epidemiology of tuberculosis. Res Microbiol 1992; 143:385–391
    [Google Scholar]
  46. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30:2114–2120
    [Google Scholar]
  47. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46
    [Google Scholar]
  48. Lu J, Breitwieser FP, Thielen P, Salzberg SL. Bracken: estimating species abundance in metagenomics data. PeerJ Comput Sci 2017; 3:e104
    [Google Scholar]
  49. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760
    [Google Scholar]
  50. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079
    [Google Scholar]
  51. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011; 27:2987–2993
    [Google Scholar]
  52. Price-Carter M, Brauning R, de Lisle GW, Livingstone P, Neill M et al. Whole Genome Sequencing for Determining the Source of Mycobacterium bovis Infections in Livestock Herds and Wildlife in New Zealand. Frontiers in Veterinary Science 2018; 5:272
    [Google Scholar]
  53. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genomics 2016; 4:e000056
    [Google Scholar]
  54. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274
    [Google Scholar]
  55. Letunic I, Bork P. Interactive tree of life (iTOL) V3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245
    [Google Scholar]
  56. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic Acids Res 2019; 47:5539–5549
    [Google Scholar]
  57. Xia E, Teo Y-Y, Ong RT-H. SpoTyping: fast and accurate in silico Mycobacterium spoligotyping from sequence reads. Genome Med 2016; 8:19
    [Google Scholar]
  58. Smith NH, Upton P. Naming spoligotype patterns for the RD9-deleted lineage of the Mycobacterium tuberculosis complex; www.Mbovis.org. Infect Genet Evol 2012; 12:873–876 [View Article]
    [Google Scholar]
  59. Faksri K, Xia E, Tan JH, Teo Y-Y, Ong RT-H. In silico region of difference (RD) analysis of Mycobacterium tuberculosis complex from sequence reads using RD-Analyzer. BMC Genomics 2016; 17:847
    [Google Scholar]
  60. Team RC R: A Language and Environment for Statistical Computing Vienna, Austria: 2013
    [Google Scholar]
  61. Kahle D, Wickham H. ggmap: spatial visualization with ggplot2. R J 2013; 5:144
    [Google Scholar]
  62. Wickham H. ggplot2: Elegant Graphics for Data Analysis Springer-Verlag New York: 2016
    [Google Scholar]
  63. Hamilton N. contourer: Contouring of non-regular three-dimensional data; 2015 https://CRAN.R-project.org/package=contoureR
  64. Hijmans RJ, Williams E, Vennes C. 2019; Geosphere: spherical trigonometry. https://CRAN.R-project.org/package=geosphere
  65. Chessel D, Dufour AB, Thioulouse J. The ade4 package - I : One-table methods. R news 2004; 4:5–10
    [Google Scholar]
  66. Dray S, Dufour A-B. The ade4 Package: Implementing the Duality Diagram for Ecologists. J Stat Softw 2007; 22:
    [Google Scholar]
  67. Dray S, Dufour AB, Chessel D. The ADE4 package — II: Two-table and K-table methods. R news 2007; 7:47–52
    [Google Scholar]
  68. Bougeard S, Dray S. Supervised Multiblock Analysis in R with the ade4 Package. J Stat Softw 2018; 86:
    [Google Scholar]
  69. Csardi G, Nepusz T. The igraph software package for complex network research. InterJournal. Complex Systems 2006; 1695:
    [Google Scholar]
  70. Pedersen TL. ggraph: An implementation of grammar of graphics for graphs and networks; 2020 https://CRAN.R-project.org/package=ggraph
  71. Sanabria L, Lagrave L, Nishibe C, Ribas ACA, Zumárraga MJ. Draft genome sequences of two Mycobacterium bovis strains isolated from beef cattle in paraguay. Genome Announc 2017; 5:
    [Google Scholar]
  72. Dippenaar A, Parsons SDC, Miller MA, Hlokwe T, Gey van Pittius NC. Progenitor strain introduction of Mycobacterium bovis at the wildlife-livestock interface can lead to clonal expansion of the disease in a single ecosystem. Infect Genet Evol 2017; 51:235–238
    [Google Scholar]
  73. Sandoval-Azuara SE, Muñiz-Salazar R, Perea-Jacobo R, Robbe-Austerman S, Perera-Ortiz A. Whole genome sequencing of Mycobacterium bovis to obtain molecular fingerprints in human and cattle isolates from Baja California, Mexico. Int J Infect Dis 2017; 63:48–56
    [Google Scholar]
  74. Andrievskaia O, Duceppe M-O, Lloyd D. Genome sequences of five Mycobacterium bovis strains isolated from farmed animals and wildlife in Canada. Genome Announc 2018; 6:e00258–18
    [Google Scholar]
  75. Panossian B, Salloum T, Araj GF, Khazen G, Tokajian S. First insights on the genetic diversity of MDR Mycobacterium tuberculosis in Lebanon. BMC Infect Dis 2018; 18:710
    [Google Scholar]
  76. Perea Razo CA, Rodríguez Hernández E, Ponce SIR, Milián Suazo F, Robbe-Austerman S. Molecular epidemiology of cattle tuberculosis in Mexico through whole-genome sequencing and spoligotyping. Plos One 2018; 13:e0201981
    [Google Scholar]
  77. Revell LJ. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 2012; 3:217–223 [View Article]
    [Google Scholar]
  78. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the beast 1.7. Mol Biol Evol 2012; 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  79. Kass RE, Raftery AE. Bayes factors. J Am Stat Assoc 1995; 90:773–795 [View Article]
    [Google Scholar]
  80. Yu G, Smith DK, Zhu H, Guan Y, Lam TT. ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2017; 8:28–36
    [Google Scholar]
  81. Rieux A, Khatchikian CE. tipdatingbeast: an R package to assist the implementation of phylogenetic tip-dating tests using beast. Mol Ecol Resour 2017; 17:608–613 [View Article][PubMed]
    [Google Scholar]
  82. Zumárraga MJ, Arriaga C, Barandiaran S, Cobos-Marín L, de Waard J. Understanding the relationship between Mycobacterium bovis spoligotypes from cattle in Latin American Countries. Res Vet Sci 2013; 94:9–21
    [Google Scholar]
  83. Higino SSDS, Pinheiro SR, de Souza GO, Dib CC, do Rosário TR. Mycobacterium bovis infection in goats from the Northeast region of Brazil. Braz J Microbiol 2011; 42:1437–1439
    [Google Scholar]
  84. Parreiras PM, Andrade GI, do Nascimento TDF, Oelemann MC, Gomes HM et al. Spoligotyping and variable number tandem repeat analysis of Mycobacterium bovis isolates from cattle in Brazil. Mem Inst Oswaldo Cruz 2012; 107:64–73 [View Article][PubMed]
    [Google Scholar]
  85. Cazola DdeO, Jorge KdosSG, Zumárraga MJ, Souza-Filho AF, Araújo FR et al. Identificação e genotipagem de Mycobacterium bovis em bovinos positivos no teste intradérmico para tuberculose em Mato Grosso do Sul. Pesq Vet Bras 2015; 35:141–147 [View Article]
    [Google Scholar]
  86. Rocha VCF, de Figueiredo SC, Rosales CAR, de Hildebrand e Grisi Filho JH, Keid LB et al. Molecular discrimination of Mycobacterium bovis in São Paulo, Brazil. Vector Borne Zoonotic Dis 2013; 13:17–21 [View Article][PubMed]
    [Google Scholar]
  87. Alzamora Filho F, Vasconcellos SEG, Gomes HM, Cavalcante MP, Suffys PN. Múltiplas estirpes de isolados de Mycobacterium bovis identificados por tipagem molecular em bovinos abatidos em matadouros-frigoríficos. Pesqui Veterinária Bras 2014; 34:103–108
    [Google Scholar]
  88. Carvalho RCT, Vasconcellos SEG, Issa M de A, Soares Filho PM, Mota P. Molecular typing of Mycobacterium bovis from cattle reared in Midwest Brazil. Plos One 2016; 11:e0162459
    [Google Scholar]
  89. Ramos DF, Silva ABS, Fagundes MQ, von Groll A, da SPEA. Molecular typing of Mycobacterium bovis isolated in the south of Brazil. Braz J Microbiol 2014; 45:657–660
    [Google Scholar]
  90. ÉB S, de Alencar AP, Hodon MA, Soares Filho PM, de Souza-Filho AF. Identification of clonal complexes of Mycobacterium bovis in Brazil. Arch Microbiol 2019; 201:1047–1051
    [Google Scholar]
  91. Almaw G, Mekonnen GA, Mihret A, Aseffa A, Taye H et al. Population structure and transmission of Mycobacterium bovis in Ethiopia. Microb Genom 2021; 7:000539 [View Article]
    [Google Scholar]
  92. Walker TM, CL I, Harrell RH, Evans JT, Kapatai G et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 2013; 13:137–146
    [Google Scholar]
  93. Xu Y, Cancino-Munoz I, Torres-Puente M, Villamayor LM, Borras R et al. High-resolution mapping of tuberculosis transmission: whole genome sequencing and phylogenetic modelling of a cohort from Valencia region, Spain. PLoS Med 2019; 16:e1002961
    [Google Scholar]
  94. Hatherell H-A, Colijn C, Stagg HR, Jackson C, Winter JR et al. Interpreting whole genome sequencing for investigating tuberculosis transmission: a systematic review. BMC Med 2016; 14:21 [View Article]
    [Google Scholar]
  95. Crispell J, Zadoks RN, Harris SR, Paterson B, Collins DM. Using whole genome sequencing to investigate transmission in a multi-host system: bovine tuberculosis in New Zealand. BMC Genomics 2017; 18:180
    [Google Scholar]
  96. Smith NH, Gordon SV, de la Rua-Domenech R, Clifton-Hadley RS, Hewinson RG. Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis. Nat Rev Microbiol 2006; 4:670–681
    [Google Scholar]
  97. Kao RR, Price-Carter M, Robbe-Austerman S. Use of genomics to track bovine tuberculosis transmission Rev. Sci Tech 2016; 35:241–258
    [Google Scholar]
  98. O'Hagan MJ, Matthews DI, Laird C, McDowell SW. Herd-level risk factors for bovine tuberculosis and adoption of related biosecurity measures in Northern Ireland: a case-control study. Vet J 2016; 213:26–32
    [Google Scholar]
  99. Milne G, Allen A, Graham J, Kirke R, McCormick C et al. Mycobacterium bovis population structure in cattle and local badgers: co-localisation and variation by farm type. Pathogens 2020; 9:592
    [Google Scholar]
  100. Picasso C, Alvarez J, VanderWaal KL, Fernandez F, Gil A et al. Epidemiological investigation of bovine tuberculosis outbreaks in Uruguay (2011–2013). Prev Vet Med 2017; 138:156–161 [View Article]
    [Google Scholar]
  101. Queiroz MR, Groff ACM, Silva NDS, Grisi-Filho JHH, Amaku M et al. Epidemiological status of bovine tuberculosis in the state of Rio grande do Sul, Brazil. Semina 2016; 37:3647–3658 [View Article]
    [Google Scholar]
  102. Maciel ALG, Loiko MR, Bueno TS, Moreira JG, Coppola M et al. Tuberculosis in Southern Brazilian wild boars (Sus scrofa): First epidemiological findings. Transbound Emerg Dis 2018; 65:518–526 [View Article]
    [Google Scholar]
  103. Menardo F, Duchêne S, Brites D, Gagneux S. The molecular clock of Mycobacterium tuberculosis. PLoS Pathog 2019; 15:e1008067 [View Article]
    [Google Scholar]
  104. Loiseau C, Menardo F, Aseffa A, Hailu E, Gumi B et al. An African origin for Mycobacterium bovis. Evol Med Public Health 2020; 2020:49–59 [View Article]
    [Google Scholar]
  105. Rodriguez-Campos S, Schürch AC, Dale J, Lohan AJ, Cunha MV et al. European 2 – a clonal complex of Mycobacterium bovis dominant in the Iberian Peninsula. Infect Genet Evol 2012; 12:866–872 [View Article]
    [Google Scholar]
  106. Smith NH, Berg S, Dale J, Allen A, Rodriguez S et al. European 1: A globally important clonal complex of Mycobacterium bovis. Infect Genet Evol 2011; 11:1340–1351 [View Article]
    [Google Scholar]
  107. Carneiro PAM, Kaneene JB. Bovine tuberculosis control and eradication in Brazil: lessons to learn from the US and Australia. Food Control 2018; 93:61–69 [View Article]
    [Google Scholar]
  108. Comas I, Homolka S, Niemann S, Gagneux S. Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS ONE 2009; 4:e7815 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000569
Loading
/content/journal/mgen/10.1099/mgen.0.000569
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Supplementary material 2

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error