199
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Molecular Epidemiology and Polymorphism Analysis in Drug-Resistant Genes in M. tuberculosis Clinical Isolates from Western and Northern India

, , , , , ORCID Icon, , & ORCID Icon show all
Pages 1717-1732 | Published online: 08 Apr 2022

References

  • World Health Organization. WHO Global Tuberculosis Report 2018. Geneva: World Health Organization; 2016.
  • Porwal C, Kaushik A, Makkar N, et al. Incidence and risk factors for extensively drug-resistant tuberculosis in Delhi region. PLoS One. 2013;8(2):e55299. doi:10.1371/journal.pone.0055299
  • Banerjee R, Allen J, Westenhouse J, et al. Extensively drug-resistant tuberculosis in California, 1993–2006. Clin Infect Dis. 2008;47(4):450–457. doi:10.1086/590009
  • World Health Organization. WHO Consolidated guidelines on tuberculosis. module 4: treatment - drug-resistant tuberculosis treatment. Online annexes; 2020.
  • Ramakrishna V, Singh PK, Prakash S, Jain A. Second line injectable drug resistance and associated genetic mutations in newly diagnosed cases of multidrug-resistant tuberculosis. Microb Drug Resist. 2020;26(8):1–5. doi:10.1089/mdr.2019.0215
  • Banerjee A, Dubnau E, Quemard A, et al. inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science (80-). 1994;263:227–230. doi:10.1126/science.8284673
  • Da Silva PEA, Palomino JC. Molecular basis and mechanisms of drug resistance in Mycobacterium tuberculosis: classical and new drugs. J Antimicrob Chemother. 2011;66:1417–1430. doi:10.1093/jac/dkr173
  • Yao C, Zhu T, Li Y, et al. Detection of rpoB, katG and inhA gene mutations in Mycobacterium tuberculosis clinical isolates from Chongqing as determined by microarray. Clin Microbiol Infect. 2010;16(11):1639–1643. doi:10.1111/j.1469-0691.2010.03267.x
  • Georghiou SB, Magana M, Garfein RS, Catanzaro DG, Catanzaro A, Rodwell TC. Evaluation of genetic mutations associated with Mycobacterium tuberculosis resistance to amikacin, kanamycin and capreomycin: a systematic review. PLoS One. 2012;7(3):e33275. doi:10.1371/journal.pone.0033275
  • Rodwell TC, Valafar F, Douglas J, et al. Predicting extensively drug-resistant Mycobacterium tuberculosis phenotypes with genetic mutations. J Clin Microbiol. 2014;52(3):781–789. doi:10.1128/JCM.02701-13
  • Zaunbrecher MA, Sikes RD, Metchock B, Shinnick TM, Posey JE. Overexpression of the chromosomally encoded aminoglycoside acetyltransferase eis confers kanamycin resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2009;106(47):20004–20009. doi:10.1073/pnas.0907925106
  • Islam MM, Tan Y, Hameed HMA, et al. Prevalence and molecular characterization of amikacin resistance among Mycobacterium tuberculosis clinical isolates from southern China. J Glob Antimicrob Resist. 2020;22:290–295. doi:10.1016/j.jgar.2020.02.019
  • Reeves AZ, Campbell PJ, Sultana R, et al. Aminoglycoside cross-resistance in Mycobacterium tuberculosis due to mutations in the 5’ untranslated region of whiB7. Antimicrob Agents Chemother. 2013;57(4):1857–1865. doi:10.1128/AAC.02191-12
  • Morris RP, Nguyen L, Gatfield J, et al. Ancestral antibiotic resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2005;102(34):12200–12205. doi:10.1073/pnas.0505446102
  • Maus CE, Plikaytis BB, Thomas M, Shinnick TM. Mutation of tlyA confers capreomycin resistance in mycobacterium tuberculosis mutation of tlyA confers capreomycin resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother. 2005;49(404):571–577. doi:10.1128/AAC.49.2.571
  • Johansen SK, Maus CE, Plikaytis BB, Douthwaite S. Capreomycin binds across the ribosomal subunit interface using tlyA-encoded 2’-O-methylations in 16S and 23S rRNAs. Mol Cell. 2006;23(2):173–182. doi:10.1016/j.molcel.2006.05.044
  • Sirgel FA, Warren RM, Streicher EM, Victor TC. gyrA mutations and phenotypic susceptibility levels to ofloxacin and moxifloxacin in clinical isolates of Mycobacterium tuberculosis. J Antimicrob Chemother. 2012;67(February):1088–1093. doi:10.1093/jac/dks033
  • Avalos E, Catanzaro D, Catanzaro A, et al. Frequency and geographic distribution of gyrA and gyrB mutations associated with fluoroquinolone resistance in clinical Mycobacterium tuberculosis isolates: a systematic review. PLoS One. 2015;10:1–24. doi:10.1371/journal.pone.0120470
  • Bablishvili N, Tukvadze N, Shashkina E, et al. Impact of gyrB and eis mutations in improving detection of second-line- drug resistance among Mycobacterium tuberculosis isolates from Georgia. Antimicrob Agents Chemother. 2017;61(September):1–9. doi:10.1128/AAC.01921-16
  • Ballif M, Harino P, Ley S, et al. Drug resistance-conferring mutations in Mycobacterium tuberculosis from Madang, Papua New Guinea. BMC Microbiol. 2012;12(191). doi:10.1186/1471-2180-12-191
  • Spies FS, Ribeiro AW, Ramos DF, et al. Streptomycin resistance and lineage-specific polymorphisms in Mycobacterium tuberculosis gidB gene. J Clin Microbiol. 2011;49(July 2011):2625–2630. doi:10.1128/JCM.00168-11
  • Baker L, Brown T, Maiden MC, Drobniewski F. Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis. Emerg Infect Dis. 2004;10(September):1568–1577. doi:10.3201/eid1009.040046
  • Casali N, Nikolayevskyy V, Balabanova Y, et al. Microevolution of extensively drug-resistant tuberculosis in Russia. Genome Res. 2012;22:735–745. doi:10.1101/gr.128678.111.22
  • Campbell PJ, Morlock GP, Sikes RD, 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):2032–2041. doi:10.1128/AAC.01550-10
  • Perizzolo PF, Dalla Costa ER, Ribeiro AW, et al. Characteristics of multidrug-resistant Mycobacterium tuberculosis in southern Brazil. Tuberculosis. 2012;92(1):56–59. doi:10.1016/j.tube.2011.09.008
  • Ford CB, Shah RR, Maeda MK, et al. Mycobacterium tuberculosis mutation rate estimates from different lineages predict substantial differences in the emergence of drug-resistant tuberculosis. Nat Genet. 2013;45(7):784–790. doi:10.1038/ng.2656
  • Gupta A, Kulkarni S, Rastogi N, Anupurba S. A study of Mycobacterium tuberculosis genotypic diversity & drug resistance mutations in Varanasi, north India. Ind J Med Res. 2014;139:892–902.
  • Gupta A, Prakash P, Singh SK, Anupurba S. Rapid genotypic detection of rpoB and katG gene mutations in Mycobacterium tuberculosis clinical isolates from Northern India as determined by MAS-PCR. J Clin Lab Anal. 2013;27(1):31–37. doi:10.1002/jcla.21558
  • Gupta R, Amrathlal RS, Prakash R, Jain S, Tiwari PK. Spoligotyping, phenotypic and genotypic characterization of katG, rpoB gene of M. tuberculosis isolates from Sahariya tribe of Madhya Pradesh India. J Infect Public Heal. 2019;12(3):395–402. doi:10.1016/j.jiph.2018.12.009
  • Vashistha H, Hanif M, Chopra KK, Shrivastava D, Khanna A. Genetic polymorphism of rare mutations in Mycobacterium tuberculosis-infected patients in Delhi. Biomed Biotechnol Res J. 2018;2:74–81. doi:10.4103/bbrj.bbrj
  • Gutierrez MC, Ahmed N, Willery E, et al. Predominance of ancestral lineages of Mycobacterium tuberculosis in India. Emerg Infect Dis. 2006;12:1367–1374. doi:10.3201/eid1209.050017
  • Singh UB, Suresh N, Bhanu NV, et al. Predominant tuberculosis spoligotypes, Delhi, India. Emerg Infect Dis. 2004;10(June):1138–1142. doi:10.3201/eid1006.030575
  • Singh J, Sankar MM, Kumar P, et al. Genetic diversity and drug susceptibility profile of Mycobacterium tuberculosis isolated from different regions of India. J Infect. 2015;71(2):207–219. doi:10.1016/j.jinf.2015.04.028
  • Poonawala H, Kumar N, Peacock SJ. A review of published spoligotype data indicates the diversity of Mycobacterium tuberculosis from India is under-represented in global databases. Infect Genet Evol. 2020;78(May2019):104072. doi:10.1016/j.meegid.2019.104072
  • Ajbani K, Rodrigues C, Shenai S, Mehta A. Mutation detection and accurate diagnosis of extensively drug-resistant tuberculosis: report from a tertiary care center in India. J Clin Microbiol. 2011;49(4):1588–1590. doi:10.1128/JCM.00113-11
  • Desikan P, Panwalkar N, Chaudhuri S, et al. Burden of baseline resistance of Mycobacterium tuberculosis to fluoroquinolones and second-line injectables in central India. Trans R Soc Trop Med Hyg. 2019:1–6. doi:10.1093/trstmh/trz121
  • Kaur S, Rana V, Singh P, et al. Novel mutations conferring resistance to kanamycin in Mycobacterium tuberculosis clinical isolates from Northern India. Tuberculosis. 2016;96(2016):96–101. doi:10.1016/j.tube.2015.10.012
  • Shah NS, Moodley P, Babaria P, et al. Rapid diagnosis of tuberculosis and multidrug resistance by the microscopic-observation drug-susceptibility assay. Am J Respir Crit Care Med. 2011;183(10):1427–1433. doi:10.1164/rccm.201009-1449OC
  • Dixit P, Singh U, Sharma P, Jain A. Evaluation of nitrate reduction assay, resazurin microtiter assay and microscopic observation drug susceptibility assay for first line antitubercular drug susceptibility testing of clinical isolates of M. tuberculosis. J Microbiol Methods. 2012;88(1):122–126. doi:10.1016/j.mimet.2011.11.006
  • Gikalo MB, Nosova EY, Krylova LY, Moroz AM. The role of eis mutations in the development of kanamycin resistance in Mycobacterium tuberculosis isolates from the Moscow region. J Antimicrob Chemother. 2012;67(9):2107–2109. doi:10.1093/jac/dks178
  • Martin A, Palomino JC. Rapid detection of ofloxacin resistance in Mycobacterium tuberculosis by two low-cost colorimetric methods: resazurin and nitrate reductase assays. J Clin Microbiol. 2005;43(4):1612–1616. doi:10.1128/JCM.43.4.1612
  • Aslan G, Tezcan S, Serin MS, Emekdas G. Genotypic analysis of isoniazid and rifampin resistance in drug-resistant clinical Mycobacterium tuberculosis complex isolates in southern Turkey. Jpn J Infect Dis. 2008;61(4):255–260.
  • Kamerbeek J, Schouls L, Kolk A, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35(4):907–914. doi:10.1016/S0305-4403(02
  • Couvin D, David A, Zozio T, Rastogi N. Macro-geographical specificities of the prevailing tuberculosis epidemic as seen through SITVIT2, an updated version of the Mycobacterium tuberculosis genotyping database. Infect Genet Evol. 2019;72:31–43. doi:10.1016/j.meegid.2018.12.030
  • Tang C, Reyes JF, Luciani F, Francis AR, Tanaka MM. spolTools: online utilities for analyzing spoligotypes of the Mycobacterium tuberculosis complex. Bioinformatics. 2008;24(20):2414–2415. doi:10.1093/bioinformatics/btn434
  • Sowajassatakul A, Prammananan T, Chaiprasert A, Phunpruch S. Molecular characterization of amikacin, kanamycin and capreomycin resistance in M/XDR-TB strains isolated in Thailand. BMC Microbiol. 2014;14(165):1–7. doi:10.1186/1471-2180-14-165
  • Zignol M, Cabibbe AM, Dean AS, et al. Genetic sequencing for surveillance of drug resistance in tuberculosis in highly endemic countries: a multi-country population-based surveillance study. Lancet Infect Dis. 2018;18:675–683. doi:10.1016/S1473-3099(18
  • Coll F, Phelan J, Hill-Cawthorne G, et al. Genome-wide analysis of multi- and extensively drug-resistant Mycobacterium tuberculosis. Nat Genet. 2018;50:307–316. doi:10.1038/s41588-017-0029-0
  • World Health Organization. The selection and use of essential medicines. twentieth report of the WHO expert committee 2015 (‎including 19th WHO model list of essential medicines and 5th WHO model list of essential medicines for children)‎. World Health Organization; 2012.
  • Alangaden GJ, Kreiswirth BN, Aouad A, et al. Mechanism of resistance to amikacin and kanamycin in Mycobacterium tuberculosis. Antimicrob Agents Chemother. 1998;42(5):1295–1297. doi:10.1128/AAC.42.5.1295
  • Brossier F, Pham A, Bernard C, et al. Molecular investigation of resistance to second line injectable drugs in multidrug-resistant clinical isolates of Mycobacterium tuberculosis in France. Antimicrob Agents Chemother. 2017;61(2):AAC.01299–16. doi:10.1128/AAC.01299-16
  • Du Q, Dai G, Long Q, et al. Mycobacterium tuberculosis rrs A1401G mutation correlates with high-level resistance to kanamycin, amikacin, and capreomycin in clinical isolates from mainland China. Diagn Microbiol Infect Dis. 2013;77(2):138–142. doi:10.1016/j.diagmicrobio.2013.06.031
  • Maus CE, Plikaytis BB, Shinnick TM. Molecular analysis of cross-resistance to capreomycin, kanamycin, amikacin, and viomycin in Mycobacterium tuberculosis. Antimicrob Agents Chemother. 2005;49(8):3192–3197. doi:10.1128/AAC.49.8.3192-3197.2005
  • Goyal A, Gadhavi H, Aring B, Mullan S. A study on molecular detection of mutations associated with second line anti-tuberculosis drug resistance. JAMB. 2019;19:1–7. doi:10.9734/jamb/2019/v19i130181
  • Suzuki Y, Katsukawa C, Tamaru A, et al. Detection of kanamycin-resistant Mycobacterium tuberculosis by identifying mutations in the 16S rRNA gene. J Clin Microbiol. 1998;36(5):1220–1225. doi:10.1128/JCM.36.5.1220-1225.1998
  • Ramaswamy S, Musser J. Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update. Tuber Lung Dis. 1998;79(1):3–29. doi:10.1054/tuld.1998.0002
  • Chakravorty S, Lee JJS, Cho EJ, et al. Genotypic susceptibility testing of Mycobacterium tuberculosis isolates for amikacin and kanamycin resistance by use of a rapid sloppy molecular beacon-based assay identifies more cases of low-level drug resistance than phenotypic Lowenstein-Jensen testing. J Clin Microbiol. 2015;53:43–51. doi:10.1128/JCM.02059-14
  • Fang H, Jia-yun L, Yue-yun M, Ming-quan S, Xiao-ke H. Relationship between enhanced intracellular survival gene mutation in Mycobacterium tuberculosis and aminoglycoside-resistance. Prog Mod Biomed. 2011;11(7):1213–1215.
  • Sowajassatakul A, Prammananan T, Chaiprasert A, Phunpruch S. Overexpression of eis without a mutation in promoter region of amikacin- and kanamycin-resistant Mycobacterium tuberculosis clinical strain. Ann Clin Microbiol Antimicrob. 2018;17:1–7. doi:10.1186/s12941-018-0285-6
  • Engström A, Perskvist N, Werngren J, Hoffner SE, Juréen P. Comparison of clinical isolates and in vitro selected mutants reveals that tlyA is not a sensitive genetic marker for capreomycin resistance in Mycobacterium tuberculosis. J Antimicrob Chemother. 2011;66(6):1247–1254. doi:10.1093/jac/dkr109
  • Hoshide M, Qian L, Rodrigues C, et al. Geographical differences associated with single-nucleotide polymorphisms (SNPs) in nine gene targets among resistant clinical isolates of Mycobacterium tuberculosis. J Clin Microbiol. 2014;52(5):1322–1329. doi:10.1128/JCM.00857-13
  • Ginsburg AS, Grosset JH, Bishai WR. Fluoroquinolones, tuberculosis, and resistance. Lancet Infect Dis. 2003;3:432–442. doi:10.1016/S1473-3099(03)00671-6
  • Jnawali HN, Hwang SC, Park YK, et al. Characterization of mutations in multi- and extensive drug resistance among strains of Mycobacterium tuberculosis clinical isolates in Republic Of Korea. Diagn Microbiol Infect Dis. 2013;76(2):187–196. doi:10.1016/j.diagmicrobio.2013.02.035
  • Engström A, Morcillo N, Imperiale B, Hoffner SE, Juréen P. Detection of first- and second-line drug resistance in Mycobacterium tuberculosis clinical isolates by pyrosequencing. J Clin Microbiol. 2012;50(6):2026–2033. doi:10.1128/JCM.06664-11
  • Choudhary E, Sharma R, Kumar Y, Agarwal N. Conditional silencing by CRISPRi reveals the role of DNA gyrase in formation of drug-tolerant persister population in Mycobacterium tuberculosis. Front Cell Infect Microbiol. 2019;9:1–13. doi:10.3389/fcimb.2019.00070
  • El Sahly HM, Teeter LD, Jost KC, Dunbar D, Lew J, Graviss EA. Incidence of moxifloxacin resistance in clinical Mycobacterium tuberculosis isolates in Houston, Texas. J Clin Microbiol. 2011;49:2942–2945. doi:10.1128/JCM.00231-11
  • Nosova EY, Bukatina A, Isaeva YD, Makarova MV, Yu K, Moroz AM. Analysis of mutations in the gyrA and gyrB genes and their association with the resistance of mycobacterium tuberculosis to levofloxacin, moxifloxacin and gatifloxacin. J Med Microbiol. 2013;62:108–113. doi:10.1099/jmm.0.046821-0
  • Varma-basil M, Kumar S, Arora J, et al. Comparison of spoligotyping, mycobacterial interspersed repetitive units typing and IS6110-RFLP in a study of genotypic diversity of Mycobacterium tuberculosis in Delhi, North India. Mem Inst Oswaldo Cruz. 2011;106(5):524–535. doi:10.1590/S0074-02762011000500002
  • Stavrum R, Myneedu VP, Arora VK, Ahmed N, Grewal HMS. In-depth molecular characterization of Mycobacterium tuberculosis from New Delhi - Predominance of drug resistant isolates of the “modern” (TbD1-) type. PLoS One. 2009;4:2–8. doi:10.1371/journal.pone.0004540
  • Singh UB, Arora J, Suresh N, et al. Genetic biodiversity of Mycobacterium tuberculosis isolates from patients with pulmonary tuberculosis in India. Infect Genet Evol. 2007;7(2007):441–448. doi:10.1016/j.meegid.2007.01.003
  • Mathuria JP, Srivastava GN, Sharma P, et al. Prevalence of Mycobacterium tuberculosis Beijing genotype and its association with drug resistance in North India. J Infect Public Heal. 2017;10(4):409–414. doi:10.1016/j.jiph.2016.06.007
  • Chatterjee A, D’Souza D, Vira T, et al. Strains of Mycobacterium tuberculosis from Western Maharashtra, India, exhibit a high degree of diversity and strain-specific associations with drug resistance, cavitary disease, and treatment failure. J Clin Microbiol. 2010;48:3593–3599. doi:10.1128/JCM.00430-10
  • Kulkarni S, Sola C, Filliol I, Rastogi N, Kadival G. Spoligotyping of Mycobacterium tuberculosis isolates from patients with pulmonary tuberculosis in Mumbai, India. Res Microbiol. 2005;156:588–596. doi:10.1016/j.resmic.2005.01.005
  • Pandey P, Bhatnagar AK, Mohan A, et al. Mycobacterium tuberculosis polyclonal infections through treatment and recurrence. PLoS One. 2020;15(8):1–15. doi:10.1371/journal.pone.0237345
  • Kargarpour Kamakoli M, Khanipour S, Hadifar S, et al. Challenge in direct Spoligotyping of Mycobacterium tuberculosis: a problematic issue in the region with high prevalence of polyclonal infections. BMC Res Notes. 2018;11(1):1–6. doi:10.1186/s13104-018-3579-z
  • Masoud K, Araj GF, Reslan L, et al. Spoligotyping of Mycobacterium tuberculosis isolates using Luminex®based method in Lebanon. J Infect Dev Count. 2020;14(8):878–885. doi:10.3855/jidc.12072