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

Eurosurveillance

Volumn 22, Issue 2, 2017, Pages

  Fiebig, Lena ^a   Kohl, T A ^b   Popovici, O ^c   Muhlenfeld M ^d   Indra, A ^e   Homorodean, D ^f   Chiotan, D ^g   Richter, E ^h   Rusch Gerdes S ^b   Schmidgruber, B ⁱ   Beckert, P ^b,j   Hauer, B ^a   Niemann, S ^b,j   Allerberger, F ^e   Haas, W ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

^b RESEARCH CENTER BORSTEL   (Germany)

^c NATIONAL INSTITUTE OF PUBLIC HEALTH   (Romania)

^d Local Public Health Office Ingolstadt   (Germany)

^e AUSTRIAN AGENCY FOR HEALTH AND FOOD SAFETY   (Austria)

^f Pneumology Clinic   (Romania)

^g Thoracic Surgery Dept   (Romania)

^h MVZ Labor Dr Limbach   (Germany)

ⁱ Municipal Department 15 Public Health Services of the City of Vienna   (Austria)

^j Deutsches Zentrum für Infektionsforschung DZIF   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; AUSTRIA; BACTERIAL GENOME; BACTERIUM ISOLATE; CLINICAL ARTICLE; DISEASE SURVEILLANCE; DRUG SENSITIVITY; GENOTYPE; GERMANY; HUMAN; INTERNATIONAL COOPERATION; MIDDLE AGED; MOLECULAR DIAGNOSTICS; MULTIDRUG RESISTANT TUBERCULOSIS; NONHUMAN; ROMANIA; SEQUENCE ALIGNMENT; SPUTUM ANALYSIS; WHOLE GENOME SEQUENCING; DNA SEQUENCE; DRUG EFFECTS; EPIDEMIC; FEMALE; GENETICS; ISOLATION AND PURIFICATION; MOLECULAR EVOLUTION; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS, MULTIDRUG-RESISTANT; VARIABLE NUMBER OF TANDEM REPEAT;

ADULT; AGED; AUSTRIA; DISEASE OUTBREAKS; EVOLUTION, MOLECULAR; FEMALE; GENOME, BACTERIAL; GENOTYPE; GERMANY; HUMANS; MIDDLE AGED; MINISATELLITE REPEATS; MYCOBACTERIUM TUBERCULOSIS; ROMANIA; SEQUENCE ANALYSIS, DNA; TUBERCULOSIS, MULTIDRUG-RESISTANT;

EID: 85010601214     PISSN: 1025496X     EISSN: 15607917     Source Type: Journal    
DOI: 10.2807/1560-7917.ES.2017.22.2.30439     Document Type: Article

References (44)

1. World Health Organization (WHO). Global tuberculosis report 2015. Geneva: WHO; 2015. WHO/HTM/TB/2015.22. Available from: http://apps.who.int/iris/bitstream/10665/191102/1/9789241565059_eng.pdf
2. European Centre for Disease Prevention and Control (ECDC)/WHO Regional Office for Europe. Tuberculosis surveillance and monitoring in Europe 2016. Stockholm: ECDC; 2016. Available from: http://ecdc.europa.eu/en/publications/_layouts/forms/Publication_DispForm.aspx?List=4f55ad51-4aed-4d32-b960-af70113dbb90&ID=1452
3. Balabanova Y, Ignatyeva O, Fiebig L, Riekstina V, Danilovits M, Jaama K, et al. Survival of patients with multidrug-resistant tuberculosis in Eastern Europe: what makes a difference? Thorax. 2016;71(9):854-61.
4. Niemann S, Köser CU, Gagneux S, Plinke C, Homolka S, Bignell H, et al. Genomic diversity among drug sensitive and multidrug resistant isolates of Mycobacterium tuberculosis with identical DNA fingerprints. PLoS One. 2009;4(10):e7407. DOI: 10.1371/journal.pone.0007407
5. 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. DOI: 10.1371/journal.pmed.1001387
6. Kato-Maeda M, Ho C, Passarelli B, Banaei N, Grinsdale J, Flores L, et al. Use of whole genome sequencing to determine the microevolution of Mycobacterium tuberculosis during an outbreak. PLoS One. 2013;8(3):e58235. DOI: 10.1371/journal.pone.0058235
7. Schürch AC, Kremer K, Daviena O, Kiers A, Boeree MJ, Siezen RJ, et al. High-resolution typing by integration of genome sequencing data in a large tuberculosis cluster. J Clin Microbiol. 2010;48(9):3403-6. DOI: 10.1128/JCM.00370-10
8. Campbell PJ, Morlock GP, Sikes RD, Dalton TL, Metchock B, Starks AM, et al. Molecular detection of mutations associated with first- and second-line drug resistance compared with conventional drug susceptibility testing of Mycobacterium tuberculosis. Antimicrob Agents Chemother. 2011;55(5):2032-41. DOI: 10.1128/AAC.01550-10
9. Comas I, Borrell S, Roetzer A, Rose G, Malla B, Kato-Maeda M, et al. Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat Genet. 2011;44(1):106-10. DOI: 10.1038/ng.1038
10. Walker TM, Kohl TA, Omar SV, Hedge J, Del Ojo Elias C, Bradley P, et al. Modernizing Medical Microbiology (MMM) Informatics Group. Whole-genome sequencing for prediction of Mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study. Lancet Infect Dis. 2015;15(10):1193-202. DOI: 10.1016/S1473-3099(15)00062-6
11. Outhred AC, Jelfs P, Suliman B, Hill-Cawthorne GA, Crawford AB, Marais BJ, et al. Added value of whole-genome sequencing for management of highly drug-resistant TB. J Antimicrob Chemother. 2015;70(4):1198-202.
12. 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. DOI: 10.1056/NEJMoa1003176
13. Stucki D, Ballif M, Bodmer T, Coscolla M, Maurer AM, Droz S, et al. Tracking a tuberculosis outbreak over 21 years: strain-specific single-nucleotide polymorphism typing combined with targeted whole-genome sequencing. J Infect Dis. 2015;211(8):1306-16.
14. Köser CU, Ellington MJ, Cartwright EJP, Gillespie SH, Brown NM, Farrington M, et al. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog. 2012;8(8):e1002824. DOI: 10.1371/journal.ppat.1002824
15. 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. DOI: 10.1111/1469-0691.12183
16. Lambregts-van Weezenbeek CS, Sebek MM, van Gerven PJ, de Vries G, Verver S, Kalisvaart NA, et al. Tuberculosis contact investigation and DNA fingerprint surveillance in The Netherlands: 6 years’ experience with nation-wide cluster feedback and cluster monitoring. Int J Tuberc Lung Dis. 2003;7(12) Suppl 3;S463-70.
17. Mears J, Abubakar I, Crisp D, Maguire H, Innes JA, Lilley M, et al. Prospective evaluation of a complex public health intervention: lessons from an initial and follow-up cross-sectional survey of the tuberculosis strain typing service in England. BMC Public Health. 2014;14(1):1023. DOI: 10.1186/1471-2458-14-1023
18. Centers for Disease Prevention and Control (CDC). TB genotyping information management system (TB GIMS). Atlanta: CDC. [Accessed: 31 March 2016]. Available from: http://www.cdc.gov/tb/programs/genotyping/tbgims/default.htm
19. De Beer JL, Kodmon C, van der Werf MJ, van Ingen J, van Soolingen D. 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. DOI: 10.2807/1560-7917.ES2014.19.11.20742
20. Canetti G, Fox W, Khomenko A, Mahler HT, Menon NK, Mitchison DA, et al. Advances in techniques of testing mycobacterial drug sensitivity, and the use of sensitivity tests in tuberculosis control programmes. Bull World Health Organ. 1969;41(1):21-43.
21. van Embden JD, Cave MD, Crawford JT, Dale JW, Eisenach KD, Gicquel B, et al. Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol. 1993;31(2):406-9.
22. Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35(4):907-14.
23. Blom J, Jakobi T, Doppmeier D, Jaenicke S, Kalinowski J, Stoye J, et al. Exact and complete short-read alignment to microbial genomes using Graphics Processing Unit programming. Bioinformatics. 2011;27(10):1351-8. DOI: 10.1093/bioinformatics/btr151
24. 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. DOI: 10.1016/S1473-3099(12)70277-3
25. Feuerriegel S, Oberhauser B, George AG, Dafae F, Richter E, Rüsch-Gerdes S, et al. Sequence analysis for detection of first-line drug resistance in Mycobacterium tuberculosis strains from a high-incidence setting. BMC Microbiol. 2012;12(1):90. DOI: 10.1186/1471-2180-12-90
26. Marttila HJ, Soini H, Huovinen P, Viljanen MK. katG mutations in isoniazid-resistant Mycobacterium tuberculosis isolates recovered from Finnish patients. Antimicrob Agents Chemother. 1996;40(9):2187-9.
27. Miotto P, Cabibbe AM, Feuerriegel S, Casali N, Drobniewski F, Rodionova Y, et al. Mycobacterium tuberculosis pyrazinamide resistance determinants: a multicenter study. MBio. 2014;5(5):e01819-14. DOI: 10.1128/mBio.01819-14
28. Plinke C, Cox HS, Zarkua N, Karimovich HA, Braker K, Diel R, et al. embCAB sequence variation among ethambutol-resistant Mycobacterium tuberculosis isolates without embB306 mutation. J Antimicrob Chemother. 2010;65(7):1359-67. DOI: 10.1093/jac/dkq120
29. DeBarber AE, Mdluli K, Bosman M, Bekker LG, Barry CE. Ethionamide activation and sensitivity in multidrug-resistant Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2000;97(17):9677-82. DOI: 10.1073/pnas.97.17.9677
30. Rengarajan J, Sassetti CM, Naroditskaya V, Sloutsky A, Bloom BR, Rubin EJ. The folate pathway is a target for resistance to the drug para-aminosalicylic acid (PAS) in mycobacteria. Mol Microbiol. 2004;53(1):275-82. DOI: 10.1111/j.1365-2958.2004.04120.x
31. Diel R, Loytved G, Nienhaus A, Castell S, Detjen A, Geerdes-Fenge H, et al. Neue Empfehlungen für die Umgebungsuntersuchungen bei Tuberkulose. [New recommendations for contact tracing in tuberculosis]. Gesundheitswesen. 2011;73(6):369-88. German. DOI: 10.1055/s-0030-1256574 PMID: 21695661
32. Bogyi M, Hagel E, Hirtl T, Klein JP, Rumetshofer R, Wolf K, et al. Österreichische Leitlinie zur Tuberkulose – Umgebungsuntersuchung. [Austrian guidelines for tuberculosis contact tracing]. Vienna: Bundesministerium für Gesundheit (BMG). [Accessed: 31 March 2016]. German. Available from: http://www.bmgf.gv.at/home/Leitlinie_Tuberkulose_Umgebungsuntersuchung
33. Decision No. 1082/2013/EU of the European Parliament and the council of the European Union of 22 October 2013 on serious cross-border threats to health and repealing Decision No 2119/98/EC. Offical Journal of the European Union. Luxembourg: Publications Office of the European Union. 5.11.2013:L 293. Available from: http://ec.europa.eu/health/preparedness_response/docs/decision_serious_crossborder_threats_22102013_en.pdf
34. Perez-Lago L, Comas I, Navarro Y, Gonzalez-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;209:98e108.
35. Schürch AC, Kremer K, Kiers A, Daviena O, Boeree MJ, Siezen RJ, et al. The tempo and mode of molecular evolution of Mycobacterium tuberculosis at patient-to-patient scale. Infect Genet Evol. 2010;10(1):108-14. DOI: 10.1016/j.meegid.2009.10.002
36. 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. DOI: 10.1016/S1473-3099(14)70022-2
37. Sandgren A, Schepisi MS, Sotgiu G, Huitric E, Migliori GB, Manissero D, et al. Tuberculosis transmission between foreign- and native-born populations in the EU/EEA: a systematic review. Eur Respir J. 2014;43(4):1159-71. DOI: 10.1183/09031936.00117213
38. Coscolla M, Barry PM, Oeltmann JE, Koshinsky H, Shaw T, Cilnis M, et al. Genomic epidemiology of multidrug-resistant Mycobacterium tuberculosis during transcontinental spread. J Infect Dis. 2015;212(2):302-10. DOI: 10.1093/infdis/jiv025
39. 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. DOI: 10.1128/JCM.00567-14
40. Driver CR, Macaraig M, McElroy PD, Clark C, Munsiff SS, Kreiswirth B, et al. Which patients’ factors predict the rate of growth of Mycobacterium tuberculosis clusters in an urban community? Am J Epidemiol. 2006;164(1):21-31. DOI: 10.1093/aje/kwj153
41. Kik SV, Verver S, van Soolingen D, de Haas PE, Cobelens FG, Kremer K, et al. Tuberculosis outbreaks predicted by characteristics of first patients in a DNA fingerprint cluster. Am J Respir Crit Care Med. 2008;178(1):96-104. DOI: 10.1164/rccm.200708-1256OC
42. Althomsons SP, Kammerer JS, Shang N, Navin TR. Using routinely reported tuberculosis genotyping and surveillance data to predict tuberculosis outbreaks. PLoS One. 2012;7(11):e48754. DOI: 10.1371/journal.pone.0048754
43. Oeltmann JE, Click ES, Moonan PK. Using tuberculosis patient characteristics to predict future cases with matching genotype results. Public Health Action. 2014;4(1):47-52. DOI: 10.5588/pha.13.0098
44. Dara M, de Colombani P, Petrova-Benedict R, Centis R, Zellweger JP, Sandgren A, et al. Minimum package for cross-border TB control and care in the WHO European region: a Wolfheze consensus statement. Eur Respir J. 2012;40(5):1081-90. DOI: 10.1183/09031936.00053012