Genetic Diversity of Drug-resistant Mycobacterium tuberculosis Isolates in Isfahan Province of Iran

Document Type : Original Article

Authors

Department of Microbiology, Faculty of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

Abstract

Background: Increasing drug resistance is an important factor in the complexity of tuberculosis (TB) control. The identification of disease transmission type, recurrence of a previous infection, or new transmission of the disease is the key factor in the control of TB. In this study, we aimed to identify the genetic diversity of drug-resistant Mycobacterium tuberculosis isolates in Isfahan province of Iran through the mycobacterial interspersed repetitive unit-variable number tandem repeat (MIRU-VNTR) typing method based on 24 loci. Materials and Methods: Of 300 isolates obtained from a variety of clinical specimens, 18 drug-resistance M. tuberculosis clinical isolates (resistant to a single drug to more than one drug) were collected between 2013 and 2015 from regional TB reference laboratory in Isfahan. All drug-resistance M. tuberculosis isolates were typed by 24-locus MIRU-VNTR typing. Results: The highest percentage of isolates, 38.8%, belonged to the East-Asian lineage (lineage 2), while the lineages Indo-Oceanic (lineage 1), East-African–Indian (lineage 3), and Euro-American (lineage 4) represented 5.5%, 22.2%, and 33.3%, respectively. Among the 33.3% (6/18) Euro-American strains, the Latin American– Mediterranean and Ural sub-lineage were 22.2% (4/18) and 11.1% (2/18), respectively. Conclusion: The results of this study show that the lineages of drug-resistant M. tuberculosis isolates in Isfahan province of Iran are similar to those reported in the Eastern Mediterranean region (indicative of the epidemiological relationship between the countries in the region). Continued molecular monitoring is important as it has been proposed that the genetics and evolutionary backgrounds of drug-resistant M. tuberculosis strains may have an impact on the transmissibility profile.

Keywords

1.
World Health Organization. Global Tuberculosis Report 2015: World Health Organization; 2015.  Back to cited text no. 1
    
2.
Serkani JE, Isfahani BN, Safaei HG, Kermanshahi RK, Asghari G. Evaluation of the effect of Humulus lupulus alcoholic extract on rifampin-sensitive and resistant isolates of Mycobacterium tuberculosis. Res Pharm Sci 2012;7:235-42.  Back to cited text no. 2
[PUBMED]    
3.
Barnes PF, Cave MD. Molecular epidemiology of tuberculosis. N Engl J Med 2003;349:1149-56.  Back to cited text no. 3
[PUBMED]    
4.
Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-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;44:4498-510.  Back to cited text no. 4
    
5.
Bidovec-Stojkovic U, Zolnir-Dovc M, Supply P. One year nationwide evaluation of 24-locus MIRU-VNTR genotyping on Slovenian Mycobacterium tuberculosis isolates. Respir Med 2011;105 Suppl 1:S67-73.  Back to cited text no. 5
[PUBMED]    
6.
Bouklata N, Supply P, Jaouhari S, Charof R, Seghrouchni F, Sadki K, et al. Molecular typing of Mycobacterium tuberculosis complex by 24-locus based MIRU-VNTR typing in conjunction with spoligotyping to assess genetic diversity of strains circulating in Morocco. PLoS One 2015;10:e0135695.  Back to cited text no. 6
[PUBMED]    
7.
Alonso M, Herranz M, Martínez Lirola M; INDAL-TB Group, González-Rivera M, Bouza E, García de Viedma D. Real-time molecular epidemiology of tuberculosis by direct genotyping of smear-positive clinical specimens. J Clin Microbiol 2012;50:1755-7.  Back to cited text no. 7
    
8.
Augustynowicz-Kopec E, Jagielski T, Kozinska M, Kremer K, van Soolingen D, Bielecki J, et al. Transmission of tuberculosis within family-households. J Infect 2012;64:596-608.  Back to cited text no. 8
    
9.
Prodinger WM, Polanecký V, Kozáková B, Müllerová M, Mezenský L, Kaustová J, et al. Molecular epidemiology of tuberculosis in the Czech Republic, 2004: Analysis of M. tuberculosis complex isolates originating from the city of prague, South Moravia and the Moravian-Silesian Region. Cent Eur J Public Health 2006;14:168-74.  Back to cited text no. 9
    
10.
World Health Organization. Guidelines for Surveillance of Drug Resistance in Tuberculosis. Geneva, Switzerland: World Health Organization; 2009.  Back to cited text no. 10
    
11.
Eisenach KD, Cave MD, Bates JH, Crawford JT. Polymerase chain reaction amplification of a repetitive DNA sequence specific for Mycobacterium tuberculosis. J Infect Dis 1990;161:977-81.  Back to cited text no. 11
[PUBMED]    
12.
Hunter PR. Reproducibility and indices of discriminatory power of microbial typing methods. J Clin Microbiol 1990;28:1903-5.  Back to cited text no. 12
[PUBMED]    
13.
Sola C, Filliol I, Legrand E, Lesjean S, Locht C, Supply P, et al. Genotyping of the Mycobacterium tuberculosis complex using MIRUs: Association with VNTR and spoligotyping for molecular epidemiology and evolutionary genetics. Infect Genet Evol 2003;3:125-33.  Back to cited text no. 13
    
14.
Moradi M, Arababadi MK, Hassanshahi G. Tuberculosis in the Afghan immigrant in Kerman province of Iran. J Biol Sci 2008;8:1107-9.  Back to cited text no. 14
    
15.
Merza MA, Farnia P, Tabarsi P, Khazampour M, Masjedi MR, Velayati AA. Anti-tuberculosis drug resistance and associated risk factors in a tertiary level TB center in Iran: A retrospective analysis. J Infect Dev Ctries 2011;5:511-9.  Back to cited text no. 15
    
16.
Shamaei M, Marjani M, Chitsaz E, Kazempour M, Esmaeili M, Farnia P, et al. First-line anti-tuberculosis drug resistance patterns and trends at the national TB referral center in Iran – Eight years of surveillance. Int J Infect Dis 2009;13:e236-40.  Back to cited text no. 16
    
17.
Ramazanzadeh R, Farnia P, Amirmozafari N, Ghazi F, Ghadertotonchi Z, Kamran J, et al. Comparison between molecular epidemiology, geographical regions and drug resistance in Mycobacterium tuberculosis strains isolated from Iranian and Afghan patients. Chemotherapy 2006;52:316-20.  Back to cited text no. 17
    
18.
Mirsaeidi MS, Tabarsi P, Farnia P, Ebrahimi G, Morris MW, Masjedi MR, et al. Trends of drug resistant Mycobacterium tuberculosis in a tertiary tuberculosis center in Iran. Saudi Med J 2007;28:544-50.  Back to cited text no. 18
    
19.
Allix-Béguec C, Harmsen D, Weniger T, Supply P, Niemann S. Evaluation and strategy for use of MIRU-VNTRplus, a multifunctional database for online analysis of genotyping data and phylogenetic identification of Mycobacterium tuberculosis complex isolates. J Clin Microbiol 2008;46:2692-9.  Back to cited text no. 19
    
20.
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;8:843-9.  Back to cited text no. 20
    
21.
Van Soolingen D, Qian L, de Haas PE, Douglas JT, Traore H, Portaels F, et al. Predominance of a single genotype of Mycobacterium tuberculosis in countries of East Asia. J Clin Microbiol 1995;33:3234-8.  Back to cited text no. 21
    
22.
Ritacco V, López B, Cafrune PI, Ferrazoli L, Suffys PN, Candia N, et al. Mycobacterium tuberculosis strains of the Beijing genotype are rarely observed in tuberculosis patients in South America. Mem Inst Oswaldo Cruz 2008;103:489-92.  Back to cited text no. 22
    
23.
Palittapongarnpim P, Luangsook P, Tansuphaswadikul S, Chuchottaworn C, Prachaktam R, Sathapatayavongs B. Restriction fragment length polymorphism study of Mycobacterium tuberculosis in Thailand using IS6110 as probe. Int J Tuberc Lung Dis 1997;1:370-6.  Back to cited text no. 23
    
24.
Schaaf HS, Shean K, Donald PR. Culture confirmed multidrug resistant tuberculosis: Diagnostic delay, clinical features, and outcome. Arch Dis Child 2003;88:1106-11.  Back to cited text no. 24
    
25.
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;40:1930-7.  Back to cited text no. 25
    
26.
Ramazanzadeh R, Sayhemiri K. Prevalence of Beijing family in Mycobacterium tuberculosis in world population: Systematic review and meta-analysis. Int J Mycobacteriol 2014;3:41-5.  Back to cited text no. 26
  [Full text]  
27.
Zhang J, Heng S, Le Moullec S, Refregier G, Gicquel B, Sola C, et al. A first assessment of the genetic diversity of Mycobacterium tuberculosis complex in Cambodia. BMC Infect Dis 2011;11:42.  Back to cited text no. 27
    
28.
Buu TN, Huyen MN, Lan NN, Quy HT, Hen NV, Zignol M, et al. Mycobacterium tuberculosis genotype and case notification rates, rural Vietnam, 2003-2006. Emerg Infect Dis 2009;15:1570-7.  Back to cited text no. 28
    
29.
Soini H, Pan X, Amin A, Graviss EA, Siddiqui A, Musser JM. Characterization of Mycobacterium tuberculosis isolates from patients in Houston, Texas, by spoligotyping. J Clin Microbiol 2000;38:669-76.  Back to cited text no. 29
    
30.
Ramazanzadeh R, Farnia P, Amirmozafari N. Characterization of Mycobacterium tuberculosis complex isolated from iranian and afghani patients by spoligotyping method. Braz J Microbiol 2009;40:314-20.  Back to cited text no. 30
    
31.
Haeili M, Darban-Sarokhalil D, Fooladi AA, Javadpour S, Hashemi A, Siavoshi F, et al. Spoligotyping and drug resistance patterns of Mycobacterium tuberculosis isolates from five provinces of Iran. Microbiologyopen 2013;2:988-96.  Back to cited text no. 31
    
32.
Hashemi A, Shojaei H, Heidarieh P, Aslani MM, Naser AD. Genetic diversity of Iranian clinical isolates of Mycobacterium tuberculosis. New Microbiol 2012;35:61-5.  Back to cited text no. 32
    
33.
Filliol I, Driscoll JR, van Soolingen D, Kreiswirth BN, Kremer K, Valétudie G, et al. Snapshot of moving and expanding clones of Mycobacterium tuberculosis and their global distribution assessed by spoligotyping in an international study. J Clin Microbiol 2003;41:1963-70.  Back to cited text no. 33
    
34.
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.  Back to cited text no. 34
    
35.
Elisseeff V. The Silk Roads. Highways of Culture and Commerce. New York, Paris: Berghahn, UNESCO; 2000.  Back to cited text no. 35
    
36.
Hasan Z, Tanveer M, Kanji A, Hasan Q, Ghebremichael S, Hasan R. Spoligotyping of Mycobacterium tuberculosis isolates from Pakistan reveals predominance of Central Asian Strain 1 and Beijing isolates. J Clin Microbiol 2006;44:1763-8.  Back to cited text no. 36
    
37.
Mustafa Ali R, Trovato A, Couvin D, Al-Thwani AN, Borroni E, Dhaer FH, et al. Molecular epidemiology and genotyping of Mycobacterium tuberculosis isolated in Baghdad. Biomed Res Int 2014;2014:580981.  Back to cited text no. 37
    
38.
Torkaman MR, Nasiri MJ, Farnia P, Shahhosseiny MH, Mozafari M, Velayati AA. Estimation of recent transmission of Mycobacterium tuberculosis strains among Iranian and Afghan immigrants: A cluster-based study. J Clin Diagn Res 2014;8:DC05-8.