Genomic analysis of globally diverse Mycobacterium tuberculosis strains provides insights into the emergence and spread of multidrug resistance

Nature Genetics

Volumn 49, Issue 3, 2017, Pages 395-402

  Manson, Abigail L ^a   Cohen, Keira A ^a,b,c   Abeel, Thomas ^a,d   Desjardins, Christopher A ^a   Armstrong, Derek T ^e   Barry, Clifton E ^f   Brand, Jeannette ^g   Chapman, Sinéad B ^a   Cho, Sang Nae ^h   Gabrielian, Andrei ⁱ   Gomez, James ^a   Jodals, Andreea M ^j   Joloba, Moses ^k   Jureen, Pontus ^l   Lee, Jong Seok ^h   Malinga, Lesibana ^g   Maiga, Mamoudou ^m   Nordenberg, Dale ⁿ   Noroc, Ecaterina ^o   Romancenco, Elena ^o   Salazar, Alex ^a,d   Ssengooba, Willy ^m   Velayati, A A ^p   Winglee, Kathryn ^e   Zalutskaya, Aksana ^q   Via, Laura E ^f   Cassell, Gail H ^c   Dorman, Susan E ^e   Ellner, Jerrold ^r   Farnia, Parissa ^p   Galagan, James E ^a,s   Rosenthal, Alex ⁱ   Crudu, Valeriu ^o   Homorodean, Daniela ^j   Hsueh, Po Ren ^t   Narayanan, Sujatha ^u   Pym, Alexander S ^b   Skrahina, Alena ^r   Swaminathan, Soumya ^u   Van Der Walt, Martie ^g   Alland, David ^v   Bishai, William R ^b,e   Cohen, Ted ^w,x   Hoffner, Sven ^m   Birren, Bruce W ^a   Earl, Ashlee M ^a   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b AFRICA HEALTH RESEARCH INSTITUTE   (South Africa)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^g SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

^h Yonsei University College of Medicine   (South Korea)

ⁱ NATIONAL INSTITUTES OF HEALTH   (United States)

^j Clinical Hospital of Pneumology Leon Daniello   (Romania)

^k MAKERERE UNIVERSITY   (Uganda)

^l SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^m Sociétés   (Mali)

ⁿ Novasano Health and Science   (United States)

^o Microbiology and Morphology Laboratory   (Moldova)

^p SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^q Republican Scientific and Practical Center for Pulmonology and Tuberculosis   (Belarus)

^r BOSTON MEDICAL CENTER   (United States)

^s BOSTON UNIVERSITY   (United States)

^t NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^u NATIONAL INSTITUTE FOR RESEARCH IN TUBERCULOSIS   (India)

^v RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^w HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^x YALE UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ETHAMBUTOL; ETHIONAMIDE; ISONIAZID; KANAMYCIN; KATG PROTEIN; OFLOXACIN; PYRAZINAMIDE; RIFAMPICIN; SERINE; STREPTOMYCIN; THYROXINE; BACTERIAL PROTEIN; CATALASE; KATG PROTEIN, MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSTATIC AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM ISOLATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC BACKGROUND; GENOMICS; HUMAN; MOLECULAR DIAGNOSIS; MULTIDRUG RESISTANCE; MULTIDRUG RESISTANT TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; WHOLE GENOME SEQUENCING; DRUG EFFECTS; GENETIC POLYMORPHISM; GENETICS; MUTATION; PROCEDURES; TUBERCULOSIS, MULTIDRUG-RESISTANT;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CATALASE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENOMICS; HUMANS; ISONIAZID; MUTATION; MYCOBACTERIUM TUBERCULOSIS; POLYMORPHISM, GENETIC; RIFAMPIN; TUBERCULOSIS, MULTIDRUG-RESISTANT;

EID: 85009773526     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3767     Document Type: Article

References (75)

1. Farmer, P. et al. The dilemma of MDR-TB in the global era. Int. J. Tuberc. Lung Dis. 2, 869-876 (1998).
2. World Health Organization. Global Tuberculosis Report 2015 (World Health Organization, Geneva, Switzerland, 2015).
3. Awofeso, N. Antituberculosis medication side effects constitute major factor for poor adherence to tuberculosis treatment. Bull. World Health Organ. 86, B-D (2008).
4. Pietersen, E. et al. Long-term outcomes of patients with extensively drug-resistant tuberculosis in South Africa: a cohort study. Lancet 383, 1230-1239 (2014).
5. Boehme, C.C. et al. Rapid molecular detection of tuberculosis and rifampin resistance. N. Engl. J. Med. 363, 1005-1015 (2010).
6. Cohen, K. et al. Evolution of extensively drug-resistant tuberculosis over four decades revealed by whole-genome sequencing of Mycobacterium tuberculosis from KwaZulu-Natal, South Africa. PLoS Med. 12, e1001880 (2015).
7. Eldholm, V. et al. Four decades of transmission of a multidrug-resistant Mycobacterium tuberculosis outbreak strain. Nat. Commun. 6, 7119 (2015).
8. Izu, A., Cohen, T. & Degruttola, V. Bayesian estimation of mixture models with prespecified elements to compare drug resistance in treatment-naive and experienced tuberculosis cases. PLoS Comput. Biol. 9, e1002973 (2013).
9. Gegia, M., Winters, N., Benedetti, A., van Soolingen, D. & Menzies, D. Treatment of isoniazid-resistant tuberculosis with first-line drugs: a systematic review and meta-analysis. Lancet Infect. Dis. http://dx.doi.org/10.1016/S1473-3099(16)30407-8 (2016).
10. Biek, R. et al. Whole-genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badger populations. PLoS Pathog. 8, e1003008 (2012).
11. Blouin, Y. et al. Significance of the identification in the Horn of Africa of an exceptionally deep branching Mycobacterium tuberculosis clade. PLoS One 7, e52841 (2012).
12. Bryant, J.M. et al. Inferring patient-to-patient transmission of Mycobacterium tuberculosis from whole-genome sequencing data. BMC Infect. Dis. 13, 110 (2013).
13. Casali, N. et al. Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nat. Genet. 46, 279-286 (2014).
14. Clark, T.G. et al. Elucidating emergence and transmission of multidrug-resistant tuberculosis in treatment-experienced patients by whole-genome sequencing. PLoS One 8, e83012 (2013).
15. Comas, I. et al. Out-of-Africa migration and neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat. Genet. 45, 1176-1182 (2013).
16. Gardy, J.L. et al. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N. Engl. J. Med. 364, 730-739 (2011).
17. Guerra-Assunção, J.A. et al. Recurrence due to relapse or re-infection with Mycobacterium tuberculosis: a whole-genome sequencing approach in a large, population-based cohort with a high HIV infection prevalence and active follow-up. J. Infect. Dis. 211, 1154-1163 (2015).
18. Merker, M. et al. Evolutionary history and global spread of the Mycobacterium tuberculosis Beijing lineage. Nat. Genet. 47, 242-249 (2015).
19. Perdigão, J. et al. Unraveling Mycobacterium tuberculosis genomic diversity and evolution in Lisbon, Portugal, a highly drug-resistant setting. BMC Genomics 15, 991 (2014).
20. Walker, T.M. et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect. Dis. 13, 137-146 (2013).
21. Zhang, H. et al. Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat. Genet. 45, 1255-1260 (2013).
22. Winglee, K. et al. Whole-genome sequencing of Mycobacterium africanum strains from Mali provides insights into the mechanisms of geographic restriction. PLoS Negl. Trop. Dis. 10, e0004332 (2016).
23. Wollenberg, K.R. et al. Whole-genome sequencing of Mycobacterium tuberculosis provides insight into the evolution and genetic composition of drug-resistant tuberculosis in Belarus. J. Clin. Microbiol. http://dx.doi.org/10.1128/JCM.02116-16 (2016).
24. Gagneux, S. et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 103, 2869-2873 (2006).
25. Yimer, S.A. et al. Mycobacterium tuberculosis lineage 7 strains are associated with prolonged patient delay in seeking treatment for pulmonary tuberculosis in Amhara region, Ethiopia. J. Clin. Microbiol. 53, 1301-1309 (2015).
26. O'Reilly, L.M. & Daborn, C.J. The epidemiology of Mycobacterium bovis infections in animals and man: a review. Tuber. Lung Dis. 76 (Suppl. 1), 1-46 (1995).
27. Desjardins, C.A. et al. Novel d-cycloserine resistance mechanism in Mycobacterium tuberculosis revealed by whole-genome analysis. Nat. Genet. 48, 544-551 (2016).
28. Ma, Z., Lienhardt, C., McIlleron, H., Nunn, A.J. & Wang, X. Global tuberculosis drug development pipeline: the need and the reality. Lancet 375, 2100-2109 (2010).
29. Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973 (2012).
30. Cattamanchi, A. et al. Clinical characteristics and treatment outcomes of patients with isoniazid-monoresistant tuberculosis. Clin. Infect. Dis. 48, 179-185 (2009).
31. Velayati, A.A. et al. High prevalance of rifampin-monoresistant tuberculosis: a retrospective analysis among Iranian pulmonary tuberculosis patients. Am. J. Trop. Med. Hyg. 90, 99-105 (2014).
32. Johnsson, K. & Schultz, P.G. Mechanistic studies of the oxidation of isoniazid by the catalase peroxidase from Mycobacterium tuberculosis. J. Am. Chem. Soc. 116, 7425-7426 (1994).
33. Rozwarski, D.A., Grant, G.A., Barton, D.H., Jacobs, W.R. Jr. & Sacchettini, J.C. Modification of the NADH of the isoniazid target (InhA) from Mycobacterium tuberculosis. Science 279, 98-102 (1998).
34. Quémard, A. et al. Enzymatic characterization of the target for isoniazid in Mycobacterium tuberculosis. Biochemistry 34, 8235-8241 (1995).
35. Marrakchi, H., Lanéelle, G. & Quémard, A. InhA, a target of the antituberculous drug isoniazid, is involved in a mycobacterial fatty acid elongation system, FAS-II. Microbiology 146, 289-296 (2000).
36. Sassetti, C.M., Boyd, D.H. & Rubin, E.J. Genes required for mycobacterial growth defined by high-density mutagenesis. Mol. Microbiol. 48, 77-84 (2003).
37. Bergval, I.L., Schuitema, A.R., Klatser, P.R. & Anthony, R.M. Resistant mutants of Mycobacterium tuberculosis selected in vitro do not reflect the in vivo mechanism of isoniazid resistance. J. Antimicrob. Chemother. 64, 515-523 (2009).
38. Ford, C.B. et al. Mycobacterium tuberculosis mutation rate estimates from different lineages predict substantial differences in the emergence of drug-resistant tuberculosis. Nat. Genet. 45, 784-790 (2013).
39. Bergval, I. et al. Pre-existing isoniazid resistance, but not the genotype of Mycobacterium tuberculosis, drives rifampicin resistance codon preference in vitro. PLoS One 7, e29108 (2012).
40. O'Sullivan, D.M., McHugh, T.D. & Gillespie, S.H. The effect of oxidative stress on the mutation rate of Mycobacterium tuberculosis with impaired catalase-peroxidase function. J. Antimicrob. Chemother. 62, 709-712 (2008).
41. Pym, A.S., Saint-Joanis, B. & Cole, S.T. Effect of katG mutations on the virulence of Mycobacterium tuberculosis and the implication for transmission in humans. Infect. Immun. 70, 4955-4960 (2002).
42. Salverda, M.L. et al. Initial mutations direct alternative pathways of protein evolution. PLoS Genet. 7, e1001321 (2011).
43. Ogbunugafor, C.B., Wylie, C.S., Diakite, I., Weinreich, D.M. & Hartl, D.L. Adaptive landscape by environment interactions dictate evolutionary dynamics in models of drug resistance. PLoS Comput. Biol. 12, e1004710 (2016).
44. Gumbo, T. et al. Concentration-dependent Mycobacterium tuberculosis killing and prevention of resistance by rifampin. Antimicrob. Agents Chemother. 51, 3781-3788 (2007).
45. Pasipanodya, J.G. & Gumbo, T. A new evolutionary and pharmacokinetic-pharmacodynamic scenario for rapid emergence of resistance to single and multiple antituberculosis drugs. Curr. Opin. Pharmacol. 11, 457-463 (2011).
46. Jutte, P.C., Rutgers, S.R., Van Altena, R., Uges, D.R. & Van Horn, J.R. Penetration of isoniazid, rifampicin and pyrazinamide in tuberculous pleural effusion and psoas abscess. Int. J. Tuberc. Lung Dis. 8, 1368-1372 (2004).
47. Diacon, A.H. et al. Early bactericidal activity of high-dose rifampin in patients with pulmonary tuberculosis evidenced by positive sputum smears. Antimicrob. Agents Chemother. 51, 2994-2996 (2007).
48. Long, M.W., Snider, D.E. Jr. & Farer, L.S. U.S. Public Health Service Cooperative trial of three rifampin-isoniazid regimens in treatment of pulmonary tuberculosis. Am. Rev. Respir. Dis. 119, 879-894 (1979).
49. Mitchison, D.A. Role of individual drugs in the chemotherapy of tuberculosis. Int. J. Tuberc. Lung Dis. 4, 796-806 (2000).
50. Mills, H.L., Cohen, T. & Colijn, C. Community-wide isoniazid preventive therapy drives drug-resistant tuberculosis: a model-based analysis. Sci. Transl. Med. 5, 180ra49 (2013).
51. Jindani, A. et al. High-dose rifapentine with moxifloxacin for pulmonary tuberculosis. N. Engl. J. Med. 371, 1599-1608 (2014).
52. Chien, J.Y. et al. Treatment outcome of patients with isoniazid-monoresistant tuberculosis. Clin. Microbiol. Infect. 21, 59-68 (2015).
53. Fasih, N., Rafiq, Y., Jabeen, K. & Hasan, R. High isoniazid resistance rates in rifampicin-susceptible Mycobacterium tuberculosis pulmonary isolates from Pakistan. PLoS One 7, e50551 (2012).
54. Jenkins, H.E., Zignol, M. & Cohen, T. Quantifying the burden and trends of isoniazid-resistant tuberculosis, 1994-2009. PLoS One 6, e22927 (2011).
55. Lumb, R. et al. Tuberculosis in Australia: bacteriologically confirmed cases and drug resistance, 2010. A report of the Australian Mycobacterium Reference Laboratory Network. Commun. Dis. Intell. Q. Rep. 37, E40-E46 (2013).
56. Nagu, T.J. et al. Multidrug-and other forms of drug-resistant tuberculosis are uncommon among treatment-naive tuberculosis patients in Tanzania. PLoS One 10, e0118601 (2015).
57. Villegas, L. et al. Prevalence, risk factors and treatment outcomes of isoniazid-and rifampicin-monoresistant pulmonary tuberculosis in Lima, Peru. PLoS One 11, e0152933 (2016).
58. Espinal, M.A. et al. Standard short-course chemotherapy for drug-resistant tuberculosis: treatment outcomes in six countries. J. Am. Med. Assoc. 283, 2537-2545 (2000).
59. Menzies, D. et al. Standardized treatment of active tuberculosis in patients with previous treatment and/or with monoresistance to isoniazid: a systematic review and meta-analysis. PLoS Med. 6, e1000150 (2009).
60. Huyen, M.N. et al. Epidemiology of isoniazid-resistance mutations and their effect on tuberculosis treatment outcomes. Antimicrob. Agents Chemother. 57, 3620-3627 (2013).
61. Denkinger, C.M., Pai, M. & Dowdy, D.W. Do we need to detect isoniazid resistance in addition to rifampicin resistance in diagnostic tests for tuberculosis? PLoS One 9, e84197 (2014).
62. Bai, Y., Wang, Y., Shao, C., Hao, Y. & Jin, Y. GenoType MTBDRplus assay for rapid detection of multidrug resistance in Mycobacterium tuberculosis: a meta-analysis. PLoS One 11, e0150321 (2016).
63. Department of Health, South Africa. Management of Drug-Resistant Tuberculosis: Policy Guidelines http://www.health-e.org.za/wp-content/uploads/2014/06/MDR-TB-Clinical-Guidelines-Updated-Jan-2013.pdf (2013).
64. Banerjee, A. et al. inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263, 227-230 (1994).
65. Larsen, M.H., Biermann, K., Tandberg, S., Hsu, T. & Jacobs, W.R. Jr. Genetic manipulation of Mycobacterium tuberculosis. Curr. Protoc. Microbiol. 6, 10A.2 (2007).
66. Walker, B.J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome-assembly improvement. PLoS One 9, e112963 (2014).
67. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
68. Salazar, A., Earl, A., Desjardins, C. & Abeel, T. Normalizing alternate representations of large sequence variants across multiple bacterial genomes. BMC Bioinformatics 16, 116 (2015).
69. Price, M.N., Dehal, P.S. & Arkin, A.P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650 (2009).
70. Walker, T.M. et al. Whole-genome sequencing for prediction of Mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study. Lancet Infect. Dis. 15, 1193-1202 (2015).
71. Farhat, M.R. et al. Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis. Nat. Genet. 45, 1183-1189 (2013).
72. Swofford, D. PAUP: Phylogenetic Analysis Using Parsimony, Version 3.0 (Illinois Natural History Survey, 1989).
73. Guerra-Assunção, J.A. et al. Large-scale whole-genome sequencing of M. tuberculosis provides insights into transmission in a high-prevalence area. eLife 4, e05166 (2015).
74. Roetzer, A. et al. Whole-genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med. 10, e1001387 (2013).
75. Ford, C.B. et al. Use of whole-genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat. Genet. 43, 482-486 (2011).