Genotyping and molecular characteristics of multidrug-resistant Mycobacterium tuberculosis isolates from China

Journal of Infection

Volumn 70, Issue 4, 2015, Pages 335-345

  Zhang, Zhijian ^a,b   Lu, Jie ^c   Liu, Min ^d   Wang, Yufeng ^b   Qu, Geping ^a   Li, Hongxia ^a   Wang, Jichun ^b   Pang, Yu ^a,b   Liu, Changting ^a   Zhao, Yanlin ^b  

^a CHINESE PLA GENERAL HOSPITAL   (China)

^b CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d Liaoning Provincial Center for Disease Control and Prevention   (China)

Author keywords

Genotyping; Multidrug resistant; Mycobacterium tuberculosis

Indexed keywords

ISONIAZID; KANAMYCIN; OFLOXACIN; RIFAMPICIN; STREPTOMYCIN; BACTERIAL PROTEIN; CATALASE; INHA PROTEIN, MYCOBACTERIUM; KATG PROTEIN, MYCOBACTERIUM TUBERCULOSIS; OXIDOREDUCTASE; RPOB PROTEIN, MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSTATIC AGENT;

ADULT; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CHINA; CONTROLLED STUDY; DNA SEQUENCE; GENE MUTATION; GENOTYPE; HUMAN; INHA GENE; KATG GENE; MULTIDRUG RESISTANT TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXYR AHPC GENE; POPULATION STRUCTURE; PROMOTER REGION; RPOB GENE; YOUNG ADULT; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; MULTIDRUG RESISTANCE; MULTIPLEX POLYMERASE CHAIN REACTION; MUTATION; PHYLOGENY;

ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; CATALASE; CHINA; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENETIC VARIATION; GENOTYPE; ISONIAZID; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; MULTIPLEX POLYMERASE CHAIN REACTION; MUTATION; MYCOBACTERIUM TUBERCULOSIS; OXIDOREDUCTASES; PHYLOGENY; RIFAMPIN; SEQUENCE ANALYSIS, DNA; TUBERCULOSIS, MULTIDRUG-RESISTANT;

EID: 84926083623     PISSN: 01634453     EISSN: 15322742     Source Type: Journal    
DOI: 10.1016/j.jinf.2014.11.008     Document Type: Article

References (57)

1. Gandhi N.R., Nunn P., Dheda K., Schaaf H.S., Zignol M., van Soolingen D., et al. Multidrug-resistant and extensively drug-resistant tuberculosis: a threat to global control of tuberculosis. Lancet 2010, 375:1830-1843.
2. Zhao Y., Xu S., Wang L., Chin D.P., Wang S., Jiang G., et al. National survey of drug-resistant tuberculosis in China. N Engl J Med 2012, 366:2161-2170.
3. World Health Oragnization Global tuberculosis report 2012, World Health Organization, Geneva, Switherland.
4. Pang Y., Zhou Y., Wang S., Lu J., Lu B., He G., et al. A novel method based on high resolution melting (HRM) analysis for MIRU-VNTR genotyping of Mycobacterium tuberculosis. J Microbiol Methods 2011, 86:291-297.
5. Mathema B., Kurepina N.E., Bifani P.J., Kreiswirth B.N. Molecular epidemiology of tuberculosis: current insights. Clin Microbiol Rev 2006, 19:658-685.
6. Rosas S., Bravo J., Gonzalez F., de Moreno N., Sanchez J., Gavilan R.G., et al. High clustering rates of multidrug-resistant Mycobacterium tuberculosis genotypes in panama. BMC Infect Dis 2013, 13:442.
7. Yuan X., Zhang T., Kawakami K., Zhu J., Zheng W., Li H., et al. Genotyping and clinical characteristics of multidrug and extensively drug-resistant tuberculosis in a tertiary caretuberculosis hospital in China. BMC Infect Dis 2013, 13:315.
8. Yasmin M., Gomgnimbou M.K., Siddiqui R.T., Refrégier G., Sola C. Multi-drug resistant Mycobacterium tuberculosis complex genetic diversity and clues on recent transmission in Punjab, Pakistan 2014, 27:6-14.
9. Zhao M., Li X., Xu P., Shen X., Gui X., Wang L., et al. Transmission of MDR and XDR tuberculosis in Shanghai, China. PLoS One 2009, 4:e4370.
10. Wang J., Liu Y., Zhang C.L., Ji B.Y., Zhang L.Z., Shao Y.Z., et al. Genotypes and characteristics of clustering and drug susceptibility of Mycobacterium tuberculosis isolates collected in Heilongjiang Province, China. J Clin Microbiol 2011, 49:1354-1362.
11. Liang Q.F., Pang Y., Chen Q.Y., Lin S.F., Lin J., Zhao Y., et al. Genetic profile of tuberculosis among the migrant population in Fujian Province, China. Int J Tuberc Lung Dis 2013, 17:655-661.
12. Ramaswamy S., Musser J.M. Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update. Tuber Lung Dis 1998, 79:3-29.
13. Almeida Da Silva P.E., Palomino J.C. Molecular basis and mechanisms of drug resistance in Mycobacterium tuberculosis: classical and new drugs. J Antimicrob Chemother 2011, 66:1417-1430.
14. Pang Y., Liu G., Wang Y., Zheng S., Zhao Y.L. Combining COLD-PCR and high-resolution melt analysis for rapid detection of low-level, rifampin-resistant mutations in Mycobacterium tuberculosis. J Microbiol Methods 2013, 93:32-36.
15. Valvatne H., Syre H., Kross M., Stavrum R., Ti T., Phyu S., et al. Isoniazid and rifampicin resistance-associated mutations in Mycobacterium tuberculosis isolates from Yangon, Myanmar: implications for rapid molecular testing. J Antimicrob Chemother 2009, 64:694-701.
16. van Soolingen D., de Haas P.E., van Doorn H.R., Kuijper E., Rinder H., Borgdorff M.W. Mutations at amino acid position 315 of the katG gene are associated with high-level resistance to isoniazid, other drug resistance, and successful transmission of Mycobacterium tuberculosis in the Netherlands. J Infect Dis 2000, 182:1788-1790.
17. Wright A., Zignol M., Van Deun A., Falzon D., Gerdes S.R., Feldman K., et al. Epidemiology of antituberculosis drug resistance 2002-07: an updated analysis of the global project on anti-tuberculosis drug resistance surveillance. Lancet 2009, 373:1861-1873.
18. Espinal M.A., Laszlo A., Simonsen L., Boulahbal F., Kim S.J., Reniero A., et al. Global trends in resistance to antituberculosis drugs. World Health Organization-International Union against tuberculosis and lung disease working group on anti-tuberculosis drug resistance surveillance. N Engl J Med 2001, 344:1294-1303.
19. World Health Oragnization Multidrug and externsively drug-resistant tuberculosis: 2010 global report on survilliance and response 2010, World Health Organization, Geneva, Switherland.
20. Pang Y., Zhou Y., Zhao B., Liu G., Jiang G., Xia H., et al. Spoligotyping and drug resistance analysis of Mycobacterium tuberculosis strains from national survey in China. PLoS One 2012, 7:e32976.
21. Zhang Z., Lu J., Wang Y., Pang Y., Zhao Y. Prevalence and molecular characterization of fluoroquinolone-resistant Mycobacterium tuberculosis isolates in China. Antimicrob Agents Chemother 2014, 58:364-369.
22. Supply P., Allix C., Lesjean S., Cardoso-Oelemann M., Rusch-Gerdes S., Willery E., et al. Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 2006, 44:4498-4510.
23. Zhang D., An J., Wang J., Hu C., Wang Z., Zhang R., et al. Molecular typing and drug susceptibility of Mycobacterium tuberculosis isolates from Chongqing municipality, China. Infect Genet Evol 2013, 13:310-316.
24. Chen Q., Pang Y., Liang Q., Lin S., Wang Y., Lin J., et al. Molecular characteristics of MDR Mycobacterium tuberculosis strains isolated in Fujian, China. Tuberc (Edinb) 2014, 94(2):159-161.
25. Glynn J.R., Whiteley J., Bifani P.J., Kremer K., van Soolingen D. Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review. Emerg Infect Dis 2002, 8:843-849.
26. Parwati I., van Crevel R., van Soolingen D. Possible underlying mechanisms for successful emergence of the Mycobacterium tuberculosis Beijing genotype strains. Lancet Infect Dis 2010, 10:103-111.
27. Mokrousov I., Jiao W.W., Sun G.Z., Liu J.W., Valcheva V., Li M., et al. Evolution of drug resistance in different sublineages of Mycobacterium tuberculosis Beijing genotype. Antimicrob Agents Chemother 2006, 50:2820-2823.
28. Mokrousov I., Ly H.M., Otten T., Lan N.N., Vyshnevskyi B., Hoffner S., et al. Origin and primary dispersal of the Mycobacterium tuberculosis Beijing genotype: clues from human phylogeography. Genome Res 2005, 15:1357-1364.
29. Yu X.L., Wen Z.L., Chen G.Z., Li R., Ding B.B., Yao Y.F., et al. Molecular characterization of multidrug-resistant Mycobacterium tuberculosis isolated from south-central in China. J Antibiot (Tokyo) 2014, 67:291-297.
30. Zhang D., An J., Wang Y., Pang Y. Genetic diversity of multidrug-resistant tuberculosis in a resource-limited region of China. Int J Infect Dis 2014, 29:7-11.
31. Zhao L.L., Chen Y., Liu H.C., Xia Q., Wu X.C., Sun Q., et al. Molecular characterization of multidrug-resistant Mycobacterium tuberculosis isolates from China. Antimicrob Agents Chemother 2014, 58(4):1997-2005.
32. Almeida D., Rodrigues C., Ashavaid T.F., Lalvani A., Udwadia Z.F., Mehta A. High incidence of the Beijing genotype among multidrug-resistant isolates of Mycobacterium tuberculosis in a tertiary care center in Mumbai, India. Clin Infect Dis 2005, 40:881-886.
33. Sun Y.J., Lee A.S., Wong S.Y., Heersma H., Kremer K., van Soolingen D., et al. Genotype and phenotype relationships and transmission analysis of drug-resistant tuberculosis in Singapore. Int J Tuberc Lung Dis 2007, 11:436-442.
34. Duong D.A., Nguyen T.H., Nguyen T.N., Dai V.H., Dang T.M., Vo S.K., et al. Beijing genotype of Mycobacterium tuberculosis is significantly associated with high-level fluoroquinolone resistance in Vietnam. Antimicrob Agents Chemother 2009, 53:4835-4839.
35. Mokrousov I., Otten T., Manicheva O., Potapova Y., Vishnevsky B., Narvskaya O., et al. Molecular characterization of ofloxacin-resistant Mycobacterium tuberculosis strains from Russia. Antimicrob Agents Chemother 2008, 52:2937-2939.
36. Yang C., Luo T., Sun G., Qiao K., DeRiemer K., Mei J., et al. Mycobacterium tuberculosis Beijing strains favor transmission but not drug resistance in China. Clin Infect Dis 2012, 55:1179-1187.
37. Devaux I., Kremer K., Heersma H., Van Soolingen D. Clusters of multidrug-resistant Mycobacterium tuberculosis cases, Europe. Emerg Infect Dis 2009, 15:1052-1060.
38. Mokrousov I., Narvskaya O., Otten T., Vyazovaya A., Limeschenko E., Steklova L., et al. Phylogenetic reconstruction within Mycobacterium tuberculosis Beijing genotype in northwestern Russia. Res Microbiol 2002, 153:629-637.
39. Hanekom M., van der Spuy G.D., Streicher E., Ndabambi S.L., McEvoy C.R., Kidd M., et al. A recently evolved sublineage of the Mycobacterium tuberculosis Beijing strain family is associated with an increased ability to spread and cause disease. J Clin Microbiol 2007, 45:1483-1490.
40. Chang J.R., Lin C.H., Tsai S.F., Su I.J., Tseng F.C., Chen Y.T., et al. Genotypic analysis of genes associated with transmission and drug resistance in the Beijing lineage of Mycobacterium tuberculosis. Clin Microbiol Infect 2011, 17:1391-1396.
41. Wada T., Fujihara S., Shimouchi A., Harada M., Ogura H., Matsumoto S., et al. High transmissibility of the modern Beijing Mycobacterium tuberculosis in homeless patients of Japan. Tuberc (Edinb) 2009, 89:252-255.
42. Kremer K., van-der-Werf M.J., Au B.K., Anh D.D., Kam K.M., van-Doorn H.R., et al. Vaccine-induced immunity circumvented by typical Mycobacterium tuberculosis Beijing strains. Emerg Infect Dis 2009, 15:335-339.
43. Gagneux S., DeRiemer K., Van T., Kato-Maeda M., Jong B., Narayanan S., et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 2006, 103:2869-2873.
44. Kato-Maeda M., Gao Q., Small P.M. Microarray analysis of pathogens and their interaction with hosts. Cell Microbiol 2001, 3:713-719.
45. Gagneux S., Small P.M. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 2007, 7:328-337.
46. Poudel A., Nakajima C., Fukushima Y., Suzuki H., Pandey B.D., Maharjan B., et al. Molecular characterization of multidrug-resistant Mycobacterium tuberculosis isolated in Nepal. Antimicrob Agents Chemother 2012, 56:2831-2836.
47. Suresh N., Singh U.B., Arora J., Pant H., Seth P., Sola C., et al. rpoB gene sequencing and spoligotyping of multidrug-resistant Mycobacterium tuberculosis isolates from India. Infect Genet Evol 2006, 6:474-483.
48. Luo T., Zhao M., Li X., Xu P., Gui X., Pickerill S., et al. Selection of mutations to detect multidrug-resistant Mycobacterium tuberculosis strains in Shanghai, China. Antimicrob Agents Chemother 2010, 54:1075-1081.
49. Hillemann D., Kubica T., Rusch-Gerdes S., Niemann S. Disequilibrium in distribution of resistance mutations among Mycobacterium tuberculosis Beijing and non-Beijing strains isolated from patients in Germany. Antimicrob Agents Chemother 2005, 49:1229-1231.
50. Lipin M.Y., Stepanshina V.N., Shemyakin I.G., Shinnick T.M. Association of specific mutations in katG, rpoB, rpsL and rrs genes with spoligotypes of multidrug-resistant Mycobacterium tuberculosis isolates in Russia. Clin Microbiol Infect 2007, 13:620-626.
51. Yuan X., Zhang T., Kawakami K., Zhu J., Li H., Lei J., et al. Molecular characterization of multidrug- and extensively drug-resistant Mycobacterium tuberculosis strains in Jiangxi, China. J Clin Microbiol 2012, 50:2404-2413.
52. Mokrousov I., Narvskaya O., Otten T., Limeschenko E., Steklova L., Vyshnevskiy B. High prevalence of KatG Ser315Thr substitution among isoniazid-resistant Mycobacterium tuberculosis clinical isolates from northwestern Russia, 1996 to 2001. Antimicrob Agents Chemother 2002, 46:1417-1424.
53. Kelley C.L., Rouse D.A., Morris S.L. Analysis of ahpC gene mutations in isoniazid-resistant clinical isolates of Mycobacterium tuberculosis. Antimicrob Agents Chemother 1997, 41:2057-2058.
54. Rinder H., Thomschke A., Rusch-Gerdes S., Bretzel G., Feldmann K., Rifai M., et al. Significance of ahpC promoter mutations for the prediction of isoniazid resistance in Mycobacterium tuberculosis. Eur J Clin Microbiol Infect Dis 1998, 17:508-511.
55. Pang Y., Xia H., Zhang Z., Li J., Dong Y., Li Q., et al. Multicenter evaluation of genechip for detection of multidrug-resistant Mycobacterium tuberculosis. J Clin Microbiol 2013, 51:1707-1713.
56. Barnard M., Warren R., Gey Van Pittius N., van Helden P., Bosman M., Streicher E., et al. Genotype MTBDRsl line probe assay shortens time to diagnosis of extensively drug-resistant tuberculosis in a high-throughput diagnostic laboratory. Am J Respir Crit Care Med 2012, 186:1298-1305.
57. Louw G.E., Warren R.M., Gey van Pittius N.C., McEvoy C.R., Van Helden P.D., Victor T.C. A balancing act: efflux/influx in mycobacterial drug resistance. Antimicrob Agents Chemother 2009, 53:3181-3189.