Frontiers of Medicine

, Volume 12, Issue 1, pp 92–97 | Cite as

Associations between Mycobacterium tuberculosis Beijing genotype and drug resistance to four first-line drugs: a survey in China

  • Haican Liu
  • Yuanyuan Zhang
  • Zhiguang Liu
  • Jinghua Liu
  • Yolande Hauck
  • Jiao Liu
  • Haiyan Dong
  • Jie Liu
  • Xiuqin Zhao
  • Bing Lu
  • Yi Jiang
  • Gilles Vergnaud
  • Christine Pourcel
  • Kanglin Wan
Research Article

Abstract

Investigations on the genetic diversity of Mycobacterium tuberculosis in China have shown that Beijing genotype strains play a dominant role. To study the association between the M. tuberculosis Beijing genotype and the drug-resistance phenotype, 1286 M. tuberculosis clinical isolates together with epidemiological and clinical information of patients were collected from the center for tuberculosis (TB) prevention and control or TB hospitals in Beijing municipality and nine provinces or autonomous regions in China. Drug resistance testing was conducted on all the isolates to the four first-line anti-TB drugs (isoniazid, rifampicin, streptomycin, and ethambutol). A total of 585 strains were found to be resistant to at least one of the four anti-TB drugs. The Beijing family strains consisted of 499 (53.20%) drug-sensitive strains and 439 (46.80%) drug-resistant strains, whereas the non-Beijing family strains comprised 202 (58.05%) drug-sensitive strains and 146 (41.95%) drug-resistant strains. No significant difference was observed in prevalence (χ2= 2.41, P > 0.05) between the drug-resistant and drugsensitive strains among the Beijing family strains. Analysis of monoresistance, multidrug-resistant TB, and geographic distribution of drug resistance did not find any relationships between the M. tuberculosis Beijing genotype and drug-resistance phenotype in China. Results confirmed that the Beijing genotype, the predominant M. tuberculosis genotype in China, was not associated with drug resistance.

Keywords

tuberculosis drug resistance genotype molecular biology 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was funded by the projects of the National Key Program of Mega Infectious Disease (Nos. 2013ZX10003006-002 and 2013ZX10003002-001) and the project of the State Key Laboratory for Infectious Disease Prevention and Control (No. 2011SKLID- 2008). The funders had no role in the study design, data collection and analysis, manuscript preparation, or decision to publish.We also thank the staff of the respective institutes in Beijing municipality, the 10 provinces, and autonomous regions in China for their excellent contribution to this study, especially for the help of Lishui Zhang (Fujian), Yunhong Tan (Hunan), Xiujun Yang (Jilin), Chongxiang Tong (Gansu), Feiying Liu (Guangxi), Yingcheng Qi (Xinjiang), Li Shi (Tibet), Xiaohui Cao (Beijing), Haitao Li (Henan), and Jun Yang (Sichuan).

References

  1. 1.
    van Soolingen D, Qian L, de Haas PE, Douglas JT, Traore H, Portaels F, Qing HZ, Enkhsaikan D, Nymadawa P, van Embden JD. Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia. J Clin Microbiol 1995; 33(12): 3234–3238PubMedPubMedCentralGoogle Scholar
  2. 2.
    Mokrousov I, Ly HM, Otten T, Lan NN, Vyshnevskyi B, Hoffner S, Narvskaya O. Origin and primary dispersal of the Mycobacterium tuberculosis Beijing genotype: clues from human phylogeography. Genome Res 2005; 15(10): 1357–1364CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Qian L, van Embden JD, van Der Zanden AG, Weltevreden EF, Duanmu H, Douglas JT. Retrospective analysis of the Beijing family of Mycobacterium tuberculosis in preserved lung tissues. J Clin Microbiol 1999; 37(2): 471–474PubMedPubMedCentralGoogle Scholar
  4. 4.
    Li WM, Wang SM, Li CY, Liu YH, Shen GM, Zhang XX, Niu TG, Gao Q, van Soolingen D, Kremer K, Duanmu HJ. Molecular epidemiology of Mycobacterium tuberculosis in China: a nationwide random survey in 2000. Int J Tuberc Lung Dis 2005; 9(12): 1314–1319PubMedGoogle Scholar
  5. 5.
    Wan K, Liu J, Hauck Y, Zhang Y, Liu J, Zhao X, Liu Z, Lu B, Dong H, Jiang Y, Kremer K, Vergnaud G, van Soolingen D, Pourcel C. Investigation on Mycobacterium tuberculosis diversity in China and the origin of the Beijing clade. PLoS One 2011; 6(12): e29190CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    WHO. Global Tuberculosis Report, 2016. 1st ed. Geneva: World Health Organization, 2016Google Scholar
  7. 7.
    Cox HS, Kubica T, Doshetov D, Kebede Y, Rüsch-Gerdess S, Niemann S. The Beijing genotype and drug resistant tuberculosis in the Aral Sea region of Central Asia. Respir Res 2005; 6(1): 134CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Sun YJ, Lee AS, Wong SY, Heersma H, Kremer K, van Soolingen D, Paton NI. Genotype and phenotype relationships and transmission analysis of drug-resistant tuberculosis in Singapore. Int J Tuberc Lung Dis 2007; 11(4): 436–442PubMedGoogle Scholar
  9. 9.
    Toungoussova OS, Sandven P, Mariandyshev AO, Nizovtseva NI, Bjune G, Caugant DA. Spread of drug-resistant Mycobacterium tuberculosis strains of the Beijing genotype in the Archangel Oblast, Russia. J Clin Microbiol 2002; 40(6): 1930–1937CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Krüüner A, Hoffner SE, Sillastu H, Danilovits M, Levina K, Svenson SB, Ghebremichael S, Koivula T, Källenius G. Spread of drug-resistant pulmonary tuberculosis in Estonia. J Clin Microbiol 2001; 39(9): 3339–3345CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Rieder HL, Chonde TM, Myking H, Urbanczik R, Laszlo A, Kim S, van Deun A. The public health service national tuberculosis reference laboratory and the national laboratory network: minimum requirements, role and operation in a low-income country. International Union Against Tuberculosis And Lung Disease (IUATLD), 1998. 68Google Scholar
  12. 12.
    Driscoll JR, Bifani PJ, Mathema B, McGarry MA, Zickas GM, Kreiswirth BN, Taber HW. Spoligologos: a bioinformatic approach to displaying and analyzing Mycobacterium tuberculosis data. Emerg Infect Dis 2002; 8(11): 1306–1309CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Filliol I, Motiwala AS, Cavatore M, Qi W, Hazbón MH, Bobadilla del Valle M, Fyfe J, García-García L, Rastogi N, Sola C, Zozio T, Guerrero MI, León CI, Crabtree J, Angiuoli S, Eisenach KD, Durmaz R, Joloba ML, Rendón A, Sifuentes-Osornio J, Ponce de León A, Cave MD, Fleischmann R, Whittam TS, Alland D. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol 2006; 188(2): 759–772CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bifani PJ, Mathema B, Kurepina NE, Kreiswirth BN. Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains. Trends Microbiol 2002; 10(1): 45–52CrossRefPubMedGoogle Scholar
  15. 15.
    Glynn JR, Whiteley J, Bifani PJ, Kremer K, van Soolingen D. Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review. Emerg Infect Dis 2002; 8(8): 843–849CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Filliol I, Driscoll JR, van Soolingen D, Kreiswirth BN, Kremer K, Valétudie G, Dang DA, Barlow R, Banerjee D, Bifani PJ, Brudey K, Cataldi A, Cooksey RC, Cousins DV, Dale JW, Dellagostin OA, Drobniewski F, Engelmann G, Ferdinand S, Gascoyne-Binzi D, Gordon M, Gutierrez MC, Haas WH, Heersma H, Kassa-Kelembho E, Ho ML, Makristathis A, Mammina C, Martin G, Moström P, Mokrousov I, Narbonne V, Narvskaya O, Nastasi A, Niobe-Eyangoh SN, Pape JW, Rasolofo-Razanamparany V, Ridell M, Rossetti ML, Stauffer F, Suffys PN, Takiff H, Texier-Maugein J, Vincent V, de Waard JH, Sola C, Rastogi N. Snapshot of moving and expanding clones of Mycobacterium tuberculosis and their global distribution assessed by spoligotyping in an international study. J Clin Microbiol 2003; 41(5): 1963–1970CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ebrahimi-Rad M, Bifani P, Martin C, Kremer K, Samper S, Rauzier J, Kreiswirth B, Blazquez J, Jouan M, van Soolingen D, Gicquel B. Mutations in putative mutator genes of Mycobacterium tuberculosis strains of the W-Beijing family. Emerg Infect Dis 2003; 9(7): 838–845CrossRefPubMedGoogle Scholar
  18. 18.
    Bifani PJ, Mathema B, Liu Z, Moghazeh SL, Shopsin B, Tempalski B, Driscol J, Frothingham R, Musser JM, Alcabes P, Kreiswirth BN. Identification of a W variant outbreak of Mycobacterium tuberculosis via population-based molecular epidemiology. JAMA 1999; 282(24): 2321–2327CrossRefPubMedGoogle Scholar
  19. 19.
    Bifani P, Mathema B, Campo M, Moghazeh S, Nivin B, Shashkina E, Driscoll J, Munsiff SS, Frothingham R, Kreiswirth BN. Molecular identification of streptomycin monoresistant Mycobacterium tuberculosis related to multidrug-resistant W strain. Emerg Infect Dis 2001; 7(5): 842–848CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Anh DD, Borgdorff MW, Van LN, Lan NT, van Gorkom T, Kremer K, van Soolingen D. Mycobacterium tuberculosis Beijing genotype emerging in Vietnam. Emerg Infect Dis 2000; 6(3): 302–305CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    van Crevel R, Parwati I, Sahiratmadja E, Marzuki S, Ottenhoff TH, Netea MG, van der Ven A, Nelwan RH, van der Meer JW, Alisjahbana B, van de Vosse E. Infection with Mycobacterium tuberculosis Beijing genotype strains is associated with polymorphisms in SLC11A1/NRAMP1 in Indonesian patients with tuberculosis. J Infect Dis 2009; 200(11): 1671–1674CrossRefPubMedGoogle Scholar
  22. 22.
    Laserson KF, Osorio L, Sheppard JD, Hernández H, Benitez AM, Brim S, Woodley CL, Hazbón MH, Villegas MV, Castaño MC, Henriquez N, Rodriguez E, Metchock B, Binkin NJ. Clinical and programmatic mismanagement rather than community outbreak as the cause of chronic, drug-resistant tuberculosis in Buenaventura, Colombia, 1998. IntJ Tuberc Lung Dis 2000; 4(7): 673–683Google Scholar
  23. 23.
    Chan MY, Borgdorff M, Yip CW, de Haas PE, Wong WS, Kam KM, van Soolingen D. Seventy percent of the Mycobacterium tuberculosis isolates in Hong Kong represent the Beijing genotype. Epidemiol Infect 2001; 127(1): 169–171CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag GmbH Germany 2018

Authors and Affiliations

  • Haican Liu
    • 1
  • Yuanyuan Zhang
    • 1
  • Zhiguang Liu
    • 1
  • Jinghua Liu
    • 1
    • 2
  • Yolande Hauck
    • 1
    • 2
  • Jiao Liu
    • 1
    • 4
  • Haiyan Dong
    • 1
  • Jie Liu
    • 1
  • Xiuqin Zhao
    • 1
  • Bing Lu
    • 1
  • Yi Jiang
    • 1
  • Gilles Vergnaud
    • 2
    • 5
  • Christine Pourcel
    • 2
  • Kanglin Wan
    • 1
    • 2
    • 3
  1. 1.State Key Laboratory for Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, National Institute for Communicable Disease Control and PreventionChinese Center for Disease Control and PreventionBeijingChina
  2. 2.Institut de Génétique et Microbiologie, UMRUniversity Paris-SudOrsayFrance
  3. 3.CNRSOrsayFrance
  4. 4.Department of Epidemiology and Health StatisticsPublic Health of Central South UniversityChangshaChina
  5. 5.DGA/MRIS-Mission pour la Recherche et l’Innovation ScientifiqueBagneuxFrance

Personalised recommendations