Frequency and distribution of tuberculosis resistance-associated mutations between Mumbai, Moldova, and Eastern Cape

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 7, 2016, Pages 3994-4004

  Georghiou, S B ^a   Seifert, M ^a   Catanzaro, D ^b   Garfein, R S ^a   Valafar, F ^c   Crudu, V ^d   Rodrigues, C ^e   Victor, T C ^f   Catanzaro, A ^a   Rodwell, T C ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF ARKANSAS   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d Microbiology and Morphology Laboratory   (Moldova)

^e P D HINDUJA NATIONAL HOSPITAL   (India)

^f STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; CAPREOMYCIN; ISONIAZID; KANAMYCIN; MOXIFLOXACIN; OFLOXACIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; BACTERIAL PROTEIN;

AHPC GENE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; CLINICAL TRIAL; CONTROLLED STUDY; DRUG RESISTANT TUBERCULOSIS; EIS GENE; EXTENSIVELY DRUG RESISTANT TUBERCULOSIS; GENE INSERTION; GYRA GENE; HUMAN; INDIA; INHA GENE; KATG GENE; LUNG TUBERCULOSIS; MOLDOVA; MOLECULAR DIAGNOSIS; MULTIDRUG RESISTANT TUBERCULOSIS; MUTATION RATE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; RPOB GENE; RRS GENE; SOUTH AFRICA; WILD TYPE; DRUG EFFECTS; GENETICS; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; MUTATION; PATHOGENICITY; TUBERCULOSIS; TUBERCULOSIS, MULTIDRUG-RESISTANT;

BACTERIAL PROTEINS; CAPREOMYCIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ISONIAZID; KANAMYCIN; MICROBIAL SENSITIVITY TESTS; MOLDOVA; MUTATION; MYCOBACTERIUM TUBERCULOSIS; RIFAMPIN; SOUTH AFRICA; TUBERCULOSIS; TUBERCULOSIS, MULTIDRUG-RESISTANT;

EID: 84977529987     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00222-16     Document Type: Article

References (48)

1. World Health Organization. 2015. Global tuberculosis report 2015. World Health Organization, Geneva, Switzerland.
2. Kent P, Kubica G. 1985. Public health mycobacteriology: a guide for the level III laboratory. US Department of Health and Human Services, Atlanta, GA.
3. Almeida Da Silva PE, Palomino JC. 2011. Molecular basis and mechanisms of drug resistance in Mycobacterium tuberculosis: classical and new drugs. J Antimicrob Chemother 66:1417-1430. http://dx.doi.org/10.1093/jac/dkr173.
4. Rodwell TC, Valafar F, Douglas J, Qian L, Garfein RS, Chawla A, Torres J, Zadorozhny V, Kim MS, Hoshide M, Catanzaro D, Jackson L, Lin G, Desmond E, Rodrigues C, Eisenach K, Victor TC, Ismail N, Crudu V, Gler MT, Catanzaro A. 2014. Predicting extensively drug-resistant Mycobacterium tuberculosis phenotypes with genetic mutations. J Clin Microbiol 52:781-789. http://dx.doi.org/10.1128/JCM.02701-13.
5. Zhang Y, Jacobs WR. 2008. Mechanisms of drug action, drug resistance and drug tolerance in Mycobacterium tuberculosis: expected phenotypes from evolutionary pressures from a highly successful pathogen, p 323-378. In Kaufmann SH, Rubin H (ed), Handbook of tuberculosis. Wiley-VCH Verlag GmbH & Co, Weinheim, Germany.
6. Hain Lifescience. 2013. Technical FAQs on Hain Genotype MTBDRplus line probe assay. Hain Lifescience, Nehren, Germany. http://www.ipaqt.org/images/ipaqt/Technical-FAQs-on-Genotype-MTBDRplus-v4.pdf.
7. Linger Y, Kukhtin A, Golova J, Perov A, Lambarqui A, Bryant L, Rudy GB, Dionne K, Fisher SL, Parrish N, Chandler DP. 2014. Simplified microarray system for simultaneously detecting rifampin, isoniazid, ethambutol, and streptomycin resistance markers in Mycobacterium tuberculosis. J Clin Microbiol 52:2100-2107. http://dx.doi.org/10.1128/JCM.00238-14.
8. Gryadunov D, Mikhailovich V, Lapa S, Roudinskii N, Donnikov M, Pan'kov S, Markova O, Kuz'min A, Chernousova L, Skotnikova O, Moroz A, Zasedatelev A, Mirzabekov A. 2005. Evaluation of hybridisation on oligonucleotide microarrays for analysis of drug-resistant Mycobacterium tuberculosis. Clin Microbiol Infect 11:531-539. http://dx.doi.org/10.1111/j.1469-0691.2005.01183.x.
9. Avalos E, Catanzaro D, Catanzaro A, Ganiats T, Brodine S, Alcaraz J, Rodwell T. 2015. Frequency and geographic distribution of gyrA and gyrB mutations associated with fluoroquinolone resistance in clinical Mycobacterium tuberculosis isolates: a systematic review. PLoS One 10:e0120470. http://dx.doi.org/10.1371/journal.pone.0120470.
10. Maruri F, Sterling TR, Kaiga AW, Blackman A, van der Heijden YF, Mayer C, Cambau E, Aubry A. 2012. A systematic review of gyrase mutations associated with fluoroquinolone-resistant Mycobacterium tuberculosis and a proposed gyrase numbering system. J Antimicrob Chemother 67:819-831. http://dx.doi.org/10.1093/jac/dkr566.
11. Seifert M, Catanzaro D, Catanzaro A, Rodwell TC. 2015. Genetic mutations associated with isoniazid resistance in Mycobacterium tuberculosis: a systematic review. PLoS One 10:e0119628. http://dx.doi.org/10.1371/journal.pone.0119628.
12. Georghiou SB, Magana M, Garfein RS, Catanzaro DG, Catanzaro A, Rodwell TC. 2012. Evaluation of genetic mutations associated with Mycobacterium tuberculosis resistance to amikacin, kanamycin and capreomycin: a systematic review. PLoS One 7:e33275. http://dx.doi.org/10.1371/journal.pone.0033275.
13. Catanzaro A, Rodwell T, Catanzaro D, Garfein RS, Jackson L, Seifert M, Georghiou SB, Trollip A, Groessl EJ, Hillery N, Crudu V, Victor T, Rodrigues C, Lin G, Valafar F, Desmond E, Eisenach K. 2015. Performance comparison of three rapid tests for the diagnosis of drug-resistant tuberculosis. PLoS One 10:e0136861. http://dx.doi.org/10.1371/journal.pone.0136861.
14. Hillery N, Groessl EJ, Trollip A, Catanzaro D, Jackson L, Rodwell TC, Garfein RS, Lin SY, Eisenach K, Ganiats TG, Park D, Valafar F, Rodrigues C, Crudu V, Victor TC, Catanzaro A. 2014. The Global Consortium for Drug-Resistant Tuberculosis Diagnostics (GCDD): design of a multi-site, head-to-head study of three rapid tests to detect extensively drug-resistant tuberculosis. Trials 15:434. http://dx.doi.org/10.1186/1745-6215-15-434.
15. Siddiqi S. 2006. MGIT procedure manual: for BACTEC MGIT 960 TB system. FIND Diagnostics.
16. World Health Organization. 2008. Policy guidance on drug-susceptibility testing (DST) of second-line antituberculosis drugs. World Health Organization, Geneva, Switzerland.
17. Lin SY, Desmond E, Bonato D, Gross W, Siddiqi S. 2009. Multicenter evaluation of Bactec MGIT 960 system for second-line drug susceptibility testing of Mycobacterium tuberculosis complex. J Clin Microbiol 47:3630-3634. http://dx.doi.org/10.1128/JCM.00803-09.
18. Rodrigues C, Jani J, Shenai S, Thakkar P, Siddiqi S, Mehta A. 2008. Drug susceptibility testing of Mycobacterium tuberculosis against second-line drugs using the Bactec MGIT 960 system. Int J Tuberc Lung Dis 12:1449-1455.
19. Lin SY, Rodwell TC, Victor TC, Rider EC, Pham L, Catanzaro A, Desmond EP. 2014. Pyrosequencing for rapid detection of extensively drug-resistant Mycobacterium tuberculosis in clinical isolates and clinical specimens. J Clin Microbiol 52:475-482. http://dx.doi.org/10.1128/JCM.01821-13.
20. Ginsburg AS, Grosset JH, Bishai WR. 2003. Fluoroquinolones, tuberculosis, and resistance. Lancet Infect Dis 3:432-442. http://dx.doi.org/10.1016/S1473-3099(03)00671-6.
21. Zaunbrecher MA, Sikes RD, Jr, Metchock B, Shinnick TM, Posey JE. 2009. Overexpression of the chromosomally encoded aminoglycoside acetyltransferase eis confers kanamycin resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 106:20004-20009. http://dx.doi.org/10.1073/pnas.0907925106.
22. Sandgren A, Strong M, Muthukrishnan P, Weiner BK, Church GM, Murray MB. 2009. Tuberculosis drug resistance mutation database. PLoS Med 6:e2. http://dx.doi.org/10.1371/journal.pmed.1000002.
23. Dhole TN, Kant S, Kumar M, Kushwaha RAS, Maurya AK, Nag VL, Singh AK, Umrao J. 2013. Use of GenoType MTBDRplus assay to assess drug resistance and mutation patterns of multidrug-resistant tuberculosis isolates in northern India. Indian J Med Microbiol 31:230-236. http://dx.doi.org/10.4103/0255-0857.115625.
24. Silva MS, Senna SG, Ribeiro MO, Valim AR, Telles MA, Kritski A, Morlock GP, Cooksey RC, Zaha A, Rossetti ML. 2003. Mutations in katG, inhA, and ahpC genes of Brazilian isoniazid-resistant isolates of Mycobacterium tuberculosis. J Clin Microbiol 41:4471-4474. http://dx.doi.org/10.1128/JCM.41.9.4471-4474.2003.
25. Kambli P, Ajbani K, Sadani M, Nikam C, Shetty A, Udwadia Z, Georghiou SB, Rodwell TC, Catanzaro A, Rodrigues C. 2015. Defining multidrug-resistant tuberculosis: correlating GenoType MTBDRplus assay results with minimum inhibitory concentrations. Diagn Microbiol Infect Dis 82:49-53. http://dx.doi.org/10.1016/j.diagmicrobio.2015.01.009.
26. Bostanabad SZ, Nojoumi SA, Jabbarzadeh E, Shekarabei M, Hoseinaei H, Rahimi MK, Ghalami M, Pourazar Dizji S, Sagalchyk ER, Titov LP. 2011. High level isoniazid resistance correlates with multiple mutation in the katG encoding catalase proxidase [sic] of pulmonary tuberculosis isolates from the frontier localities of Iran. Tuberk Toraks 59:27-35. http://dx.doi.org/10.5578/tt.761.
27. Abe C, Kobayashi I, Mitarai S, Wada M, Kawabe Y, Takashima T, Suzuki K, Sng LH, Wang S, Htay HH, Ogata H. 2008. Biological and molecular characteristics of Mycobacterium tuberculosis clinical isolates with low-level resistance to isoniazid in Japan. J Clin Microbiol 46:2263-2268. http://dx.doi.org/10.1128/JCM.00561-08.
28. Coll P, Aragon LM, Alcaide F, Espasa M, Garrigo M, Gonzalez J, Manterola JM, Orus P, Salvado M. 2005. Molecular analysis of isoniazid and rifampin resistance in Mycobacterium tuberculosis isolates recovered from Barcelona. Microb Drug Resist 11:107-114. http://dx.doi.org/10.1089/mdr.2005.11.107.
29. Pym AS, Saint-Joanis B, Cole ST. 2002. Effect of katG mutations on the virulence of Mycobacterium tuberculosis and the implication for transmission in humans. Infect Immun 70:4955-4960. http://dx.doi.org/10.1128/IAI.70.9.4955-4960.2002.
30. Ando H, Kondo Y, Suetake T, Toyota E, Kato S, Mori T, Kirikae T. 2010. Identification of katG mutations associated with high-level isoniazid resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 54:1793-1799. http://dx.doi.org/10.1128/AAC.01691-09.
31. Dalla Costa ER, Ribeiro MO, Silva MS, Arnold LS, Rostirolla DC, Cafrune PI, Espinoza RC, Palaci M, Telles MA, Ritacco V, Suffys PN, Lopes ML, Campelo CL, Miranda SS, Kremer K, da Silva PE, Fonseca LDS, Ho JL, Kritski AL, Rossetti ML. 2009. Correlations of mutations in katG, oxyR-ahpC and inhA genes and in vitro susceptibility in Mycobacterium tuberculosis clinical strains segregated by spoligotype families from tuberculosis prevalent countries in South America. BMC Microbiol 9:39. http://dx.doi.org/10.1186/1471-2180-9-39.
32. Torres JN, Paul LV, Rodwell TC, Victor TC, Amallraja AM, Elghraoui A, Goodmanson AP, Ramirez-Busby SM, Chawla A, Zadorozhny V, Streicher EM, Sirgel FA, Catanzaro D, Rodrigues C, Gler MT, Crudu V, Catanzaro A, Valafar F. 2015. Novel katG mutations causing isoniazid resistance in clinical M. tuberculosis isolates. Emerg Microbes Infect 4:e42. http://dx.doi.org/10.1038/emi.2015.42.
33. Kiepiela P, Bishop KS, Smith AN, Roux L, York DF. 2000. Genomic mutations in the katG, inhA and aphC genes are useful for the prediction of isoniazid resistance in Mycobacterium tuberculosis isolates from Kwazulu Natal, South Africa. Tuber Lung Dis 80:47-56. http://dx.doi.org/10.1054/tuld.1999.0231.
34. Sreevatsan S, Pan X, Zhang Y, Deretic V, Musser JM. 1997. Analysis of the oxyR-ahpC region in isoniazid-resistant and -susceptible Mycobacterium tuberculosis complex organisms recovered from diseased humans and animals in diverse localities. Antimicrob Agents Chemother 41:600-606.
35. Barnard M, Gey van Pittius NC, van Helden PD, Bosman M, Coetzee G, Warren RM. 2012. The diagnostic performance of the GenoType MTBDRplus version 2 line probe assay is equivalent to that of the Xpert MTB/RIF assay. J Clin Microbiol 50:3712-3716. http://dx.doi.org/10.1128/JCM.01958-12.
36. Nebenzahl-Guimaraes H, Jacobson KR, Farhat MR, Murray MB. 2014. Systematic review of allelic exchange experiments aimed at identifying mutations that confer drug resistance in Mycobacterium tuberculosis. J Antimicrob Chemother 69:331-342. http://dx.doi.org/10.1093/jac/dkt358.
37. Rigouts L, Gumusboga M, de Rijk WB, Nduwamahoro E, Uwizeye C, de Jong B, Van Deun A. 2013. Rifampin resistance missed in automated liquid culture system for Mycobacterium tuberculosis isolates with specific rpoB mutations. J Clin Microbiol 51:2641-2645. http://dx.doi.org/10.1128/JCM.02741-12.
38. Van Deun A, Aung KJ, Bola V, Lebeke R, Hossain MA, de Rijk WB, Rigouts L, Gumusboga A, Torrea G, de Jong BC. 2013. Rifampin drug resistance tests for tuberculosis: challenging the gold standard. J Clin Microbiol 51:2633-2640. http://dx.doi.org/10.1128/JCM.00553-13.
39. Singh P, Jain A, Dixit P, Prakash S, Jaiswal I, Venkatesh V, Singh M. 2015. Prevalence of gyrA and B gene mutations in fluoroquinolone-resistant and -sensitive clinical isolates of Mycobacterium tuberculosis and their relationship with MIC of ofloxacin. J Antibiot (Tokyo) 68:63-66. http://dx.doi.org/10.1038/ja.2014.95.
40. Brossier F, Veziris N, Aubry A, Jarlier V, Sougakoff W. 2010. Detection by GenoType MTBDRsl test of complex mechanisms of resistance to second-line drugs and ethambutol in multidrug-resistant Mycobacterium tuberculosis complex isolates. J Clin Microbiol 48:1683-1689. http://dx.doi.org/10.1128/JCM.01947-09.
41. Chan RC, Hui M, Chan EW, Au TK, Chin ML, Yip CK, AuYeang CK, Yeung CY, Kam KM, Yip PC, Cheng AF. 2007. Genetic and phenotypic characterization of drug-resistant Mycobacterium tuberculosis isolates in Hong Kong. J Antimicrob Chemother 59:866-873. http://dx.doi.org/10.1093/jac/dkm054.
42. Mokrousov I, Narvskaya O, Otten T, Limeschenko E, Steklova L, Vyshnevskiy B. 2002. High prevalence of KatG Ser315Thr substitution among isoniazid-resistant Mycobacterium tuberculosis clinical isolates from northwestern Russia, 1996 to 2001. Antimicrob Agents Chemother 46:1417-1424. http://dx.doi.org/10.1128/AAC.46.5.1417-1424.2002.
43. Ajbani K, Lin SY, Rodrigues C, Nguyen D, Arroyo F, Kaping J, Jackson L, Garfein RS, Catanzaro D, Eisenach K, Victor TC, Crudu V, Gler MT, Ismail N, Desmond E, Catanzaro A, Rodwell TC. 2015. Evaluation of pyrosequencing for detecting extensively drug-resistant Mycobacterium tuberculosis among clinical isolates from four high-burden countries. Antimicrob Agents Chemother 59:414-420. http://dx.doi.org/10.1128/AAC.03614-14.
44. Campbell PJ, Morlock GP, Sikes RD, Dalton TL, Metchock B, Starks AM, Hooks DP, Cowan LS, Plikaytis BB, Posey JE. 2011. Molecular detection of mutations associated with first- and second-line drug resistance compared with conventional drug susceptibility testing of Mycobacterium tuberculosis. Antimicrob Agents Chemother 55:2032-2041. http://dx.doi.org/10.1128/AAC.01550-10.
45. Kambli P, Ajbani K, Nikam C, Sadani M, Shetty A, Udwadia Z, Georghiou SB, Rodwell TC, Catanzaro A, Rodrigues C. 1 October 2015. Correlating rrs and eis promoter mutations in clinical isolates of Mycobacterium tuberculosis with phenotypic susceptibility levels to the second-line injectables. Int J Mycobacteriol http://dx.doi.org/10.1016/j.ijmyco.2015.09.001.
46. Gikalo MB, Nosova EY, Krylova LY, Moroz AM. 2012. The role of eis mutations in the development of kanamycin resistance in Mycobacterium tuberculosis isolates from the Moscow region. J Antimicrob Chemother 67:2107-2109. http://dx.doi.org/10.1093/jac/dks178.
47. Toungoussova OS, Mariandyshev AO, Bjune G, Caugant DA, Sandven P. 2005. Resistance of multidrug-resistant strains of Mycobacterium tuberculosis from the Archangel oblast, Russia, to second-line antituberculosis drugs. Eur J Clin Microbiol Infect Dis 24:202-206. http://dx.doi.org/10.1007/s10096-005-1284-z.
48. Casali N, Nikolayevskyy V, Balabanova Y, Harris SR, Ignatyeva O, Kontsevaya I, Corander J, Bryant J, Parkhill J, Nejentsev S, Horstmann RD, Brown T, Drobniewski F. 2014. Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nat Genet 46:279-286. http://dx.doi.org/10.1038/ng.2878.