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Abstract

Background

The analysis of transmission of tuberculosis (TB) is challenging in areas with a large migrant population. Standard genotyping may fail to differentiate transmission within the host country from new importations, which is key from an epidemiological perspective.

Aim

To propose a new strategy to simplify and optimise cross-border surveillance of tuberculosis and to distinguish between recent transmission in the host country and new importations

Methods

We selected 10 clusters, defined by 24-locus mycobacterial interspersed repetitive unit-variable number tandem repeat (MIRU-VNTR), from a population in Spain rich in migrants from eastern Europe, north Africa and west Africa and reanalysed 66 isolates by whole-genome sequencing (WGS). A multiplex-allele-specific PCR was designed to target strain-specific marker single nucleotide polymorphisms (SNPs), identified from WGS data, to optimise the surveillance of the most complex cluster.

Results

In five of 10 clusters not all isolates showed the short genetic distances expected for recent transmission and revealed a higher number of SNPs, thus suggesting independent importations of prevalent strains in the country of origin. In the most complex cluster, rich in Moroccan cases, a multiplex allele-specific oligonucleotide-PCR (ASO-PCR) targeting the marker SNPs for the transmission subcluster enabled us to prospectively identify new secondary cases. The ASO-PCR-based strategy was transferred and applied in Morocco, demonstrating that the strain was prevalent in the country.

Conclusion

We provide a new model for optimising the analysis of cross-border surveillance of TB transmission in the scenario of global migration.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
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/content/10.2807/1560-7917.ES.2019.24.4.1800005
2019-01-24
2024-12-31
/content/10.2807/1560-7917.ES.2019.24.4.1800005
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References

  1. de Vries G, Aldridge RW, Cayla JA, Haas WH, Sandgren A, van Hest NA, et al. Epidemiology of tuberculosis in big cities of the European Union and European Economic Area countries. Euro Surveill. 2014;19(9):20726.  https://doi.org/10.2807/1560-7917.ES2014.19.9.20726  PMID: 24626208 
  2. Diel R, Rüsch-Gerdes S, Niemann S. Molecular epidemiology of tuberculosis among immigrants in Hamburg, Germany. J Clin Microbiol. 2004;42(7):2952-60.  https://doi.org/10.1128/JCM.42.7.2952-2960.2004  PMID: 15243044 
  3. Iñigo J, García de Viedma D, Arce A, Palenque E, Herranz M, Rodríguez E, et al. Differential findings regarding molecular epidemiology of tuberculosis between two consecutive periods in the context of steady increase of immigration. Clin Microbiol Infect. 2013;19(3):292-7.  https://doi.org/10.1111/j.1469-0691.2012.03794.x  PMID: 22404140 
  4. Ospina JE, Orcau À, Millet JP, Ros M, Gil S, Caylà JABarcelona Tuberculosis Immigration Working Group. Epidemiology of Tuberculosis in Immigrants in a Large City with Large-Scale Immigration (1991-2013). PLoS One. 2016;11(10):e0164736.  https://doi.org/10.1371/journal.pone.0164736  PMID: 27749904 
  5. De Beer JL, Kodmon C, van der Werf MJ, van Ingen J, van Soolingen D, Collective the ECDC MDR-TB molecular surveillance project participants. Molecular surveillance of multi- and extensively drug-resistant tuberculosis transmission in the European Union from 2003 to 2011. Euro Surveill. 2014;19(11):20742.  https://doi.org/10.2807/1560-7917.ES2014.19.11.20742  PMID: 24679719 
  6. Lillebaek T, Andersen AB, Bauer J, Dirksen A, Glismann S, de Haas P, et al. Risk of Mycobacterium tuberculosis transmission in a low-incidence country due to immigration from high-incidence areas. J Clin Microbiol. 2001;39(3):855-61.  https://doi.org/10.1128/JCM.39.3.855-861.2001  PMID: 11230395 
  7. Martínez-Lirola M, Alonso-Rodriguez N, Sánchez ML, Herranz M, Andrés S, Peñafiel T, et al. Advanced survey of tuberculosis transmission in a complex socioepidemiologic scenario with a high proportion of cases in immigrants. Clin Infect Dis. 2008;47(1):8-14.  https://doi.org/10.1086/588785  PMID: 18484876 
  8. Alonso Rodríguez N, Chaves F, Iñigo J, Bouza E, García de Viedma D, Andrés S, et al. TB Molecular Epidemiology Study Group of Madrid. Transmission permeability of tuberculosis involving immigrants, revealed by a multicentre analysis of clusters. Clin Microbiol Infect. 2009;15(5):435-42.  https://doi.org/10.1111/j.1469-0691.2008.02670.x  PMID: 19416291 
  9. Bryant JM, Schürch AC, van Deutekom H, Harris SR, de Beer JL, de Jager V, et al. Inferring patient to patient transmission of Mycobacterium tuberculosis from whole genome sequencing data. BMC Infect Dis. 2013;13(1):110.  https://doi.org/10.1186/1471-2334-13-110  PMID: 23446317 
  10. Gardy JL, Johnston JC, Ho Sui SJ, Cook VJ, Shah L, Brodkin E, et al. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med. 2011;364(8):730-9.  https://doi.org/10.1056/NEJMoa1003176  PMID: 21345102 
  11. Roetzer A, Diel R, Kohl TA, Rückert C, Nübel U, Blom J, et al. Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med. 2013;10(2):e1001387.  https://doi.org/10.1371/journal.pmed.1001387  PMID: 23424287 
  12. Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis. 2013;13(2):137-46.  https://doi.org/10.1016/S1473-3099(12)70277-3  PMID: 23158499 
  13. Alonso-Rodriguez N, Martínez-Lirola M, Sánchez ML, Herranz M, Peñafiel T, Bonillo MC, et al. Prospective universal application of mycobacterial interspersed repetitive-unit-variable-number tandem-repeat genotyping to characterize Mycobacterium tuberculosis isolates for fast identification of clustered and orphan cases. J Clin Microbiol. 2009;47(7):2026-32.  https://doi.org/10.1128/JCM.02308-08  PMID: 19458183 
  14. Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-Gerdes S, Willery E, et al. Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2006;44(12):4498-510.  https://doi.org/10.1128/JCM.01392-06  PMID: 17005759 
  15. Stucki D, Malla B, Hostettler S, Huna T, Feldmann J, Yeboah-Manu D, et al. Two new rapid SNP-typing methods for classifying Mycobacterium tuberculosis complex into the main phylogenetic lineages. PLoS One. 2012;7(7):e41253.  https://doi.org/10.1371/journal.pone.0041253  PMID: 22911768 
  16. Carcelén M, Abascal E, Herranz M, Santantón S, Zenteno R, Ruiz Serrano MJ, et al. Optimizing and accelerating the assignation of lineages in Mycobacterium tuberculosis using novel alternative single-tube assays. PLoS One. 2017;12(11):e0186956.  https://doi.org/10.1371/journal.pone.0186956  PMID: 29091913 
  17. Pérez-Lago L, Comas I, Navarro Y, González-Candelas F, Herranz M, Bouza E, et al. Whole genome sequencing analysis of intrapatient microevolution in Mycobacterium tuberculosis: potential impact on the inference of tuberculosis transmission. J Infect Dis. 2014;209(1):98-108.  https://doi.org/10.1093/infdis/jit439  PMID: 23945373 
  18. Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet. 2013;45(10):1176-82.  https://doi.org/10.1038/ng.2744  PMID: 23995134 
  19. The R project for Statistical computing. Available from: https://www.r-project.org
  20. Coll F, McNerney R, Guerra-Assunção JA, Glynn JR, Perdigão J, Viveiros M, et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat Commun. 2014;5(1):4812.  https://doi.org/10.1038/ncomms5812  PMID: 25176035 
  21. Comas I, Hailu E, Kiros T, Bekele S, Mekonnen W, Gumi B, et al. Population Genomics of Mycobacterium tuberculosis in Ethiopia Contradicts the Virgin Soil Hypothesis for Human Tuberculosis in Sub-Saharan Africa. Curr Biol. 2015;25(24):3260-6.  https://doi.org/10.1016/j.cub.2015.10.061  PMID: 26687624 
  22. Guerra-Assunção JA, Crampin AC, Houben RM, Mzembe T, Mallard K, Coll F, et al. Large-scale whole genome sequencing of M. tuberculosis provides insights into transmission in a high prevalence area. eLife. 2015;4:e05166.  https://doi.org/10.7554/eLife.05166  PMID: 25732036 
  23. Chaoui I, Zozio T, Lahlou O, Sabouni R, Abid M, El Aouad R, et al. Contribution of spoligotyping and MIRU-VNTRs to characterize prevalent Mycobacterium tuberculosis genotypes infecting tuberculosis patients in Morocco. Infect Genet Evol. 2014;21:463-71.  https://doi.org/10.1016/j.meegid.2013.05.023  PMID: 23732366 
  24. Anderson LF, Tamne S, Brown T, Watson JP, Mullarkey C, Zenner D, et al. Transmission of multidrug-resistant tuberculosis in the UK: a cross-sectional molecular and epidemiological study of clustering and contact tracing. Lancet Infect Dis. 2014;14(5):406-15.  https://doi.org/10.1016/S1473-3099(14)70022-2  PMID: 24602842 
  25. Pedersen MK, Andersen AB, Andersen PH, Svensson E, Jensen SG, Lillebaek T. Occupational Tuberculosis in Denmark through 21 Years Analysed by Nationwide Genotyping. PLoS One. 2016;11(4):e0153668.  https://doi.org/10.1371/journal.pone.0153668  PMID: 27082745 
  26. Kamper-Jørgensen Z, Andersen AB, Kok-Jensen A, Bygbjerg IC, Andersen PH, Thomsen VO, et al. Clustered tuberculosis in a low-burden country: nationwide genotyping through 15 years. J Clin Microbiol. 2012;50(8):2660-7.  https://doi.org/10.1128/JCM.06358-11  PMID: 22675129 
  27. Stucki D, Ballif M, Egger M, Furrer H, Altpeter E, Battegay M, et al. Standard Genotyping Overestimates Transmission of Mycobacterium tuberculosis among Immigrants in a Low-Incidence Country. J Clin Microbiol. 2016;54(7):1862-70.  https://doi.org/10.1128/JCM.00126-16  PMID: 27194683 
  28. Guthrie J, Kong C, Roth D, Rodrigues M, Hoang L, Walker T, et al. Findings from whole genome sequencing of tuberculosis in a geographically large Canadian province with a diverse population. 25-28 Jun 2017. 38th Congress of the European Society of mycobacteriology.; Sibenik, Croatia. OP 29. Available from: http://vorschau.agentur-konsens.de/ESM/downloads/2017/ESM_Abstract_Book2017_final.pdf
  29. Jajou R dNH, Mulder A, Kamst M, van Hunen R, de Vries G, Anthony R, et al. VNTR typing is less reliable in predicting epidemiological links than expected, as indicated by whole genome sequencing (WGS) analysis. J Clin Microbiol. Forthcoming 2017.
  30. Walker TM, Monk P, Smith EG, Peto TE. Contact investigations for outbreaks of Mycobacterium tuberculosis: advances through whole genome sequencing. Clin Microbiol Infect. 2013;19(9):796-802.  https://doi.org/10.1111/1469-0691.12183  PMID: 23432709 
  31. Folkvardsen DB, Norman A, Andersen AB, Michael Rasmussen E, Jelsbak L, Lillebaek T. Genomic Epidemiology of a Major Mycobacterium tuberculosis Outbreak: Retrospective Cohort Study in a Low-Incidence Setting Using Sparse Time-Series Sampling. J Infect Dis. 2017;216(3):366-74.  https://doi.org/10.1093/infdis/jix298  PMID: 28666374 
  32. Kohl TA, Diel R, Harmsen D, Rothgänger J, Walter KM, Merker M, et al. Whole-genome-based Mycobacterium tuberculosis surveillance: a standardized, portable, and expandable approach. J Clin Microbiol. 2014;52(7):2479-86.  https://doi.org/10.1128/JCM.00567-14  PMID: 24789177 
  33. Cirillo DM, Cabibbe AM, De Filippo MR, Trovato A, Simonetti T, Rossolini GM, et al. Use of WGS in Mycobacterium tuberculosis routine diagnosis. Int J Mycobacteriol. 2016;5(Suppl 1):S252-3.  https://doi.org/10.1016/j.ijmyco.2016.09.053  PMID: 28043590 
  34. Walker TM, Lalor MK, Broda A, Ortega LS, Morgan M, Parker L, et al. Assessment of Mycobacterium tuberculosis transmission in Oxfordshire, UK, 2007-12, with whole pathogen genome sequences: an observational study. Lancet Respir Med. 2014;2(4):285-92.  https://doi.org/10.1016/S2213-2600(14)70027-X  PMID: 24717625 
  35. Walker TM, Merker M, Kohl TA, Crook DW, Niemann S, Peto TE. Whole genome sequencing for M/XDR tuberculosis surveillance and for resistance testing. Clin Microbiol Infect. 2017;23(3):161-6.  https://doi.org/10.1016/j.cmi.2016.10.014  PMID: 27789378 
  36. Perez-Lago L, Martinez Lirola M, Herranz M, Comas I, Bouza E, Garcia-de-Viedma D. Fast and low-cost decentralized surveillance of transmission of tuberculosis based on strain-specific PCRs tailored from whole genome sequencing data: a pilot study. Clin Microbiol Infect. 2015;21(3):249 e1-9.
  37. Pérez-Lago L, Herranz M, Comas I, Ruiz-Serrano MJ, López Roa P, Bouza E, et al. Ultrafast Assessment of the Presence of a High-Risk Mycobacterium tuberculosis Strain in a Population. J Clin Microbiol. 2016;54(3):779-81.  https://doi.org/10.1128/JCM.02851-15  PMID: 26719445 
  38. Pérez-Lago L, Martínez-Lirola M, García S, Herranz M, Mokrousov I, Comas I, et al. Urgent Implementation in a Hospital Setting of a Strategy To Rule Out Secondary Cases Caused by Imported Extensively Drug-Resistant Mycobacterium tuberculosis Strains at Diagnosis. J Clin Microbiol. 2016;54(12):2969-74.  https://doi.org/10.1128/JCM.01718-16  PMID: 27682128 
  39. Lahlou O, Millet J, Chaoui I, Sabouni R, Filali-Maltouf A, Akrim M, et al. The genotypic population structure of Mycobacterium tuberculosis complex from Moroccan patients reveals a predominance of Euro-American lineages. PLoS One. 2012;7(10):e47113.  https://doi.org/10.1371/journal.pone.0047113  PMID: 23077552 
  40. Fiebig L, Kohl TA, Popovici O, Mühlenfeld M, Indra A, Homorodean D, et al. A joint cross-border investigation of a cluster of multidrug-resistant tuberculosis in Austria, Romania and Germany in 2014 using classic, genotyping and whole genome sequencing methods: lessons learnt. Euro Surveill. 2017;22(2):30439.  https://doi.org/10.2807/1560-7917.ES.2017.22.2.30439  PMID: 28106529 
Whole genome sequencing–based analysis of tuberculosis (TB) in migrants: rapid tools for cross-border surveillance and to distinguish between recent transmission in the host country and new importations
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Estefan%C3%ADa+Abascal&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Abascal Estefanía</a>, <a href="/search?value1=Laura+P%C3%A9rez-Lago&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pérez-Lago Laura</a>, <a href="/search?value1=Miguel+Mart%C3%ADnez-Lirola&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Martínez-Lirola Miguel</a>, <a href="/search?value1=%C3%81lvaro+Chiner-Oms&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chiner-Oms Álvaro</a>, <a href="/search?value1=Marta+Herranz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Herranz Marta</a>, <a href="/search?value1=Imane+Chaoui&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chaoui Imane</a>, <a href="/search?value1=I%C3%B1aki+Comas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Comas Iñaki</a>, <a href="/search?value1=My+Driss+El+Messaoudi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">El Messaoudi My Driss</a>, <a href="/search?value1=Jos%C3%A9+Antonio+Garrido+C%C3%A1rdenas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cárdenas José Antonio Garrido</a>, <a href="/search?value1=Sheila+Santant%C3%B3n&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Santantón Sheila</a>, <a href="/search?value1=Emilio+Bouza&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bouza Emilio</a>, <a href="/search?value1=Dar%C3%ADo+Garc%C3%ADa-de-Viedma&option1=author&noRedirect=true" class="nonDisambigAuthorLink">García-de-Viedma Darío</a></span>. Whole genome sequencing–based analysis of tuberculosis (TB) in migrants: rapid tools for cross-border surveillance and to distinguish between recent transmission in the host country and new importations. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(4):pii=1800005. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.4.1800005" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.4.1800005</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 26 Dec 2017;&nbsp;&nbsp; <span class="generated">Accepted</span>: 01 Jun 2018 </span> </p>
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