Mycobacterium tuberculosis drug-resistance testing: challenges, recent developments and perspectives

Clinical Microbiology and Infection

Volumn 23, Issue 3, 2017, Pages 154-160

  Schon T ^a,b,c   Miotto, P ^d   Koser C U ^e   Viveiros, M ^c,f   Bottger E ^c,g   Cambau, E ^c,h,i,j  

^a KALMAR COUNTY HOSPITAL   (Sweden)

^b LINKÖPING UNIVERSITY   (Sweden)

^c European Society for Clinical Microbiology and Infectious Diseases (ESCMID) Study Group for Mycobacterial Infections (ESGMYC)   (Switzerland)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^g UNIVERSITY OF ZURICH   (Switzerland)

^h National Reference Center for Mycobacteria and Antimycobacterial Resistance   (France)

ⁱ HÔPITAL LARIBOISIÈRE   (France)

^j UNIVERSITÉ PARIS DESCARTES   (France)

more..

Author keywords

Antimicrobial susceptibility testing; Critical concentration; Critical proportion; Genetic resistance; Hot spot mutations; Minimum inhibitory concentration

Indexed keywords

AMIKACIN; CAPREOMYCIN; ETHAMBUTOL; ISONIAZID; KANAMYCIN; MOXIFLOXACIN; OFLOXACIN; RIFAMPICIN; RNA POLYMERASE BETA SUBUNIT; STREPTOMYCIN; DNA DIRECTED RNA POLYMERASE; TUBERCULOSTATIC AGENT;

ANTIBIOTIC RESISTANCE; EXTENSIVELY DRUG RESISTANT TUBERCULOSIS; GENOTYPE; HIGH INCOME COUNTRY; HOT SPOT MUTATION; HUMAN; LOW INCOME COUNTRY; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANT TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; REVIEW; SUSCEPTIBLE POPULATION; DRUG EFFECTS; GENETICS; GENOTYPING TECHNIQUE; MICROBIAL SENSITIVITY TEST; PROCEDURES; TRENDS;

ANTITUBERCULAR AGENTS; DNA-DIRECTED RNA POLYMERASES; DRUG RESISTANCE, BACTERIAL; GENOTYPE; GENOTYPING TECHNIQUES; HUMANS; MICROBIAL SENSITIVITY TESTS; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE;

EID: 85007273791     PISSN: 1198743X     EISSN: 14690691     Source Type: Journal    
DOI: 10.1016/j.cmi.2016.10.022     Document Type: Review

References (50)

1. [1] Marshall, G., Blacklock, J., Cameron, C., Capon, N., Cruickshank, R., Gaddum, J., et al. Streptomycin treatment of pulmonary tuberculosis. Br Med J 2 (1948), 769–782.
2. [2] Daniels, M., Fox, W., A large-scale trial of isoniazid in pulmonary tuberculosis. Proc R Soc Med, 46, 1953, 584.
3. [3] Tsukamura, M., Nakamura, E., Yoshii, S., Amano, H., Therapeutic effect of a new antibacterial substance ofloxacin (DL8280) on pulmonary tuberculosis. Am Rev Respir Dis 131 (1985), 352–356.
4. [4] Bloemberg, G.V., Keller, P.M., Stucki, D., Trauner, A., Borrell, S., Latshang, T., et al. Acquired resistance to bedaquiline and delamanid in therapy for tuberculosis. N Engl J Med 373 (2015), 1986–1988.
5. [5] Heifets, L.B., Cangelosi, G.A., Drug susceptibility testing of Mycobacterium tuberculosis: a neglected problem at the turn of the century. Int J Tuberc Lung Dis 3 (1999), 564–581.
6. [6] World Health Organization. Global tuberculosis report 2015. Available at: WHO/HTM/TB/2015.22. http://www.who.int/tb/publications/global_report/en.
7. [7] Canetti, G., Present aspects of bacterial resistance in tuberculosis. Am Rev Respir Dis 92 (1965), 687–703.
8. [8] Mitchison, D.A., Drug resistance in tuberculosis. Eur Respir J 25 (2005), 376–379.
9. [9] Heym, B., Honore, N., Truffot-Pernot, C., Banerjee, A., Schurra, C., Jacobs, W.R. Jr., et al. Implications of multidrug resistance for the future of short-course chemotherapy of tuberculosis: a molecular study. Lancet 344 (1994), 293–298.
10. [10] Perdigão, J., Macedo, R., Silva, C., Machado, D., Couto, I., Viveiros, M., et al. From multidrug-resistant to extensively drug-resistant tuberculosis in Lisbon, Portugal: the stepwise mode of resistance acquisition. J Antimicrob Chemother 68 (2013), 27–33.
11. [11] Canetti, G., Froman, S., Grosset, J., Hauduroy, P., Langerova, M., Mahler, H.T., et al. Mycobacteria: laboratory methods for testing drug sensitivity and resistance. Bull World Health Organ 29 (1963), 565–578.
12. [12] EUCAST, Workshop on recommendations for pharmaceutical companies regarding data required for new antituberculous drugs. 2014 Available at: http://www.eucast.org/mycobacteria/.
13. [13] Mitchison, D.A., What is drug resistance?. Tubercle 50:Suppl (1969), 44–47.
14. [14] Cambau, E., Rüsch-Gerdes, S., First and second line susceptibility testing for mycobacterium tuberculosis complex. Handbook on TB laboratory diagnostic methods for the European Union European Center for disease prevention and control (ECDC) ed, 2016, ECDC, Stockholm, 72–82.
15. [15] Böttger, E.C., The ins and outs of Mycobacterium tuberculosis drug susceptibility testing. Clin Microbiol Infect 17 (2011), 1128–1134.
16. [16] Cambau, E., Viveiros, M., Machado, D., Raskine, L., Ritter, C., Tortoli, E., et al. Revisiting susceptibility testing in MDR-TB by a standardized quantitative phenotypic assessment in a European multicentre study. J Antimicrob Chemother 70 (2015), 686–696.
17. [17] Olaru, I.D., Lange, C., Heyckendorf, J., Personalized medicine for patients with MDR-TB. J Antimicrob Chemother 71 (2016), 852–855.
18. [18] Springer, B., Lucke, K., Calligaris-Maibach, R., Ritter, C., Böttger, E.C., Quantitative drug susceptibility testing of Mycobacterium tuberculosis by use of MGIT 960 and EpiCenter instrumentation. J Clin Microbiol 47 (2009), 1773–1780.
19. [19] Ängeby, K., Juréen, P., Kahlmeter, G., Hoffner, S.E., Schön, T., Challenging a dogma: antimicrobial susceptibility testing breakpoints for Mycobacterium tuberculosis. Bull World Health Organ 90 (2012), 693–698.
20. [20] Kahlmeter, G., The 2014 Garrod Lecture: EUCAST—are we heading towards international agreement?. J Antimicrob Chemother 70 (2015), 2427–2439.
21. [21] CLSI, Susceptibiity testing of mycobacteria, nocardiae, and other aerobic actinomycetes; approved standard, second edition. M24-A2, vol. 31, 2010, CLSI, Wayne, PA.
22. [22] Barrera, L., Cooreman, E., de Dieu Iragena, J., Drobniewski, F., Duda, P., Havelkova, M., et al. Policy guidance on drug-susceptibility testing (DST) of second-line antituberculosis drugs. Geneva, 2008.
23. [23] Schön, T., Juréen, P., Giske, C.G., Chryssanthou, E., Sturegard, E., Werngren, J., et al. Evaluation of wild-type MIC distributions as a tool for determination of clinical breakpoints for Mycobacterium tuberculosis. J Antimicrob Chemother 64 (2009), 786–793.
24. [24] Schön, T., Juréen, P., Chryssanthou, E., Giske, C.G., Kahlmeter, G., Hoffner, S., et al. Rifampicin-resistant and rifabutin-susceptible Mycobacterium tuberculosis strains: a breakpoint artefact?. J Antimicrob Chemother 68 (2013), 2074–2077.
25. [25] Dominguez, J., Boettger, E.C., Cirillo, D., Cobelens, F., Eisenach, K.D., Gagneux, S., et al. Clinical implications of molecular drug resistance testing for Mycobacterium tuberculosis: a TBNET/RESIST-TB consensus statement. Int J Tuberc Lung Dis 20 (2016), 24–42.
26. [26] Rigouts, L., Gumusboga, M., de Rijk, W.B., Nduwamahoro, E., Uwizeye, C., de Jong, B., et al. Rifampin resistance missed in automated liquid culture system for Mycobacterium tuberculosis isolates with specific rpoB mutations. J Clin Microbiol 51 (2013), 2641–2645.
27. [27] Van Deun, A., Aung, K.J., Bola, V., Lebeke, R., Hossain, M.A., de Rijk, W.B., et al. Rifampin drug resistance tests for tuberculosis: challenging the gold standard. J Clin Microbiol 51 (2013), 2633–2640.
28. [28] Boeree, M.J., Diacon, A.H., Dawson, R., Narunsky, K., du Bois, J., Venter, A., et al. A dose-ranging trial to optimize the dose of rifampin in the treatment of tuberculosis. Am J Respir Crit Care Med 191 (2015), 1058–1065.
29. [29] Rigouts, L., Coeck, N., Gumusboga, M., de Rijk, W.B., Aung, K.J., Hossain, M.A., et al. Specific gyrA gene mutations predict poor treatment outcome in MDR-TB. J Antimicrob Chemother 71 (2016), 314–323.
30. [30] Pasipanodya, J.G., McIlleron, H., Burger, A., Wash, P.A., Smith, P., Gumbo, T., Serum drug concentrations predictive of pulmonary tuberculosis outcomes. J Infect Dis 208 (2013), 1464–1473.
31. [31] Zhang, Y., Yew, W.W., Mechanisms of drug resistance in Mycobacterium tuberculosis: update 2015. Int J Tuberc Lung Dis 19 (2015), 1276–1289.
32. [32] WHO. UNITAID Secretariat, Tuberculosis diagnostics technology and market landscape. 4th ed., 2015, WHO, Geneva.
33. [33] WHO, Automated real-time nucleic acid amplification technology for rapid and simultaneous detection of tuberculosis and rifampicin resistance: Xpert MTB/RIF assay for the: diagnosis of pulmonary and extrapulmonary TB in adults and children. Policy update, 2013, WHO, Geneva.
34. [34] Ritter, C., Lucke, K., Sirgel, F.A., Warren, R.W., van Helden, P.D., Böttger, E.C., et al. Evaluation of the AID TB resistance line probe assay for rapid detection of genetic alterations associated with drug resistance in Mycobacterium tuberculosis strains. J Clin Microbiol 52 (2014), 940–946.
35. [35] Ling, D.I., Zwerling, A.A., Pai, M., GenoType MTBDR assays for the diagnosis of multidrug-resistant tuberculosis: a meta-analysis. Eur Respir J 32 (2008), 1165–1174.
36. [36] Nathavitharana, R.R., Hillemann, D., Schumacher, S.G., Schlueter, B., Ismail, N., Omar, S.V., et al. Multicenter noninferiority evaluation of Hain GenoType MTBDRplus Version 2 and Nipro NTM+MDRTB line probe assays for detection of rifampin and isoniazid resistance. J Clin Microbiol 54 (2016), 1624–1630.
37. [37] De Beenhouwer, H., Lhiang, Z., Jannes, G., Mijs, W., Machtelinckx, L., Rossau, R., et al. Rapid detection of rifampicin resistance in sputum and biopsy specimens from tuberculosis patients by PCR and line probe assay. Tuber Lung Dis 76 (1995), 425–430.
38. [38] Denkinger, C.M., Schumacher, S.G., Boehme, C.C., Dendukuri, N., Pai, M., Steingart, K.R., Xpert MTB/RIF assay for the diagnosis of extrapulmonary tuberculosis: a systematic review and meta-analysis. Eur Respir J 44 (2014), 435–446.
39. [39] Steingart, K.R., Schiller, I., Horne, D.J., Pai, M., Boehme, C.C., Dendukuri, N., Xpert(R) MTB/RIF assay for pulmonary tuberculosis and rifampicin resistance in adults. Cochrane Database Syst Rev, 2014, CD009593.
40. [40] Andres, S., Hillemann, D., Rüsch-Gerdes, S., Richter, E., Occurrence of rpoB mutations in isoniazid-resistant but rifampin-susceptible Mycobacterium tuberculosis isolates from Germany. Antimicrob Agents Chemother 58 (2014), 590–592.
41. [41] World Health Organization, The use of molecular line probe assays for the detection of resistance to second-line antituberculosis drugs. Policy guidance, 2016, WHO, Geneva.
42. [42] Köser, C.U., Feuerriegel, S., Summers, D.K., Archer, J.A., Niemann, S., Importance of the genetic diversity within the Mycobacterium tuberculosis complex for the development of novel antibiotics and diagnostic tests of drug resistance. Antimicrob Agents Chemother 56 (2012), 6080–6087.
43. [43] Köser, C.U., Bryant, J.M., Parkhill, J., Peacock, S.J., Consequences of whiB7 (Rv3197A) mutations in Beijing genotype isolates of the Mycobacterium tuberculosis complex. Antimicrob Agents Chemother, 57, 2013, 3461.
44. [44] Streicher, E.M., Bergval, I., Dheda, K., Böttger, E.C., Gey van Pittius, N.C., Bosman, M., et al. Mycobacterium tuberculosis population structure determines the outcome of genetics-based second-line drug resistance testing. Antimicrob Agents Chemother 56 (2012), 2420–2427.
45. [45] Eilertson, B., Maruri, F., Blackman, A., Herrera, M., Samuels, D.C., Sterling, T.R., High proportion of heteroresistance in gyrA and gyrB in fluoroquinolone-resistant Mycobacterium tuberculosis clinical isolates. Antimicrob Agents Chemother 58 (2014), 3270–3275.
46. [46] Simons, S.O., van Ingen, J., van der Laan, T., Mulder, A., Dekhuijzen, P.N., Boeree, M.J., et al. Validation of pncA gene sequencing in combination with the mycobacterial growth indicator tube method to test susceptibility of Mycobacterium tuberculosis to pyrazinamide. J Clin Microbiol 50 (2012), 428–434.
47. [47] Pantel, A., Petrella, S., Veziris, N., Matrat, S., Bouige, A., Ferrand, H., et al. Description of compensatory gyrA mutations restoring fluoroquinolone susceptibility in Mycobacterium tuberculosis. J Antimicrob Chemother 71 (2016), 2428–2431.
48. [48] Fenner, L., Egger, M., Bodmer, T., Altpeter, E., Zwahlen, M., Jaton, K., et al. Effect of mutation and genetic background on drug resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 56 (2012), 3047–3053.
49. [49] Falzon, D., Mirzayev, F., Wares, F., Baena, I.G., Zignol, M., Linh, N., et al. Multidrug-resistant tuberculosis around the world: what progress has been made?. Eur Respir J 45 (2015), 150–160.
50. [50] Ahmad, S., Mokaddas, E., Al-Mutairi, N., Eldeen, H.S., Mohammadi, S., Discordance across phenotypic and molecular methods for drug susceptibility testing of drug-resistant Mycobacterium tuberculosis isolates in a low TB incidence country. PLoS One, 11, 2016, e0153563.