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Published in: BMC Infectious Diseases 1/2010

Open Access 01-12-2010 | Research article

Diversity of Mycobacterium tuberculosis genotypes circulating in Ndola, Zambia

Authors: Chanda Mulenga, Isdore C Shamputa, David Mwakazanga, Nathan Kapata, Françoise Portaels, Leen Rigouts

Published in: BMC Infectious Diseases | Issue 1/2010

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Abstract

Background

Tuberculosis (TB) is one of the major public health problems in Zambia. However, information about lineages of M. tuberculosis complex (MTBC) isolates useful for epidemiology investigations is unknown. In this study, we investigated the diversity of MTBC isolates from Ndola, a typical Zambian urbanized city with a documented high HIV prevalence.

Methods

This was part of a prospective cohort study in subjects with sputum smear-positive pulmonary TB. Spoligotyping was used to genotype the MTBC isolates and establish the circulating lineages. The 15-locus Mycobacterial Interspersed Repetitive Units - Variable Number Tandem Repeats (MIRU-VNTR) typing was used to study recent transmission.

Results

A total of 98 different spoligotypes were identified among 273 MTBC isolates. The majority (64.8%) of the isolates belonged to 9 known families, while 96 (35.2%) of the isolates were orphans. While LAM (41.8%) was the largest spoligotype family observed, most of the isolates (87.7%) belonging to the SAF1 family, with a significant portion coming from the T (13.6%), and X (5.9%) families. A few isolates (3.6%) belonged to the CAS, EAI, H, S, X1-LAM9 or U families. MIRU-VNTR typing was highly discriminatory (h = 0.988) among the 156 isolates tested in our sample, and increased the discrimination among 82 SAF1 isolates from 6 to 46 distinct patterns. In addition, 3.2% (5/156) of cases with available MIRU-VNTR results harbored more than one MTBC strain.

Conclusions

Our findings show a limited diversity of MTBC in Ndola with a high clustering rate (37.7%), which indicates that recent transmission plays an appreciable role in the dynamics of TB disease in this setting. This conclusion emphasizes the importance of early diagnosis and timely treatment. The results also confirm that MIRU-VNTR typing is suitable for studying the molecular epidemiology of TB in Ndola.
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Literature
1.
go back to reference World Health Organization: Global Tuberculosis Control WHO Report. 2009, WHO/HTM/TB/2009.411, Geneva, Switzerland, WHO World Health Organization: Global Tuberculosis Control WHO Report. 2009, WHO/HTM/TB/2009.411, Geneva, Switzerland, WHO
2.
go back to reference Central Statistical Office (CSO), Ministry of Health (MOH), Tropical Diseases Research Centre (TDRC), University of Zambia (UNZA), and Macro International Inc: Zambia Demographic and Health Survey 2007. 2009, Calverton, Maryland, USA: CSO and Macro International Inc Central Statistical Office (CSO), Ministry of Health (MOH), Tropical Diseases Research Centre (TDRC), University of Zambia (UNZA), and Macro International Inc: Zambia Demographic and Health Survey 2007. 2009, Calverton, Maryland, USA: CSO and Macro International Inc
3.
go back to reference van Embden JD, Cave MD, Crawford JT, Dale JW, Eisenach KD, Gicquel B, Hermans P, Martin C, McAdam R, Shinnick TM, Small PM: Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol. 1993, 31 (2): 406-409.PubMedPubMedCentral van Embden JD, Cave MD, Crawford JT, Dale JW, Eisenach KD, Gicquel B, Hermans P, Martin C, McAdam R, Shinnick TM, Small PM: Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol. 1993, 31 (2): 406-409.PubMedPubMedCentral
4.
go back to reference Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J: Simultaneous detection and strain differentiation of Mycobacterium tuberculosisfor diagnosis and epidemiology. J Clin Microbiol. 1997, 35 (4): 907-914.PubMedPubMedCentral Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J: Simultaneous detection and strain differentiation of Mycobacterium tuberculosisfor diagnosis and epidemiology. J Clin Microbiol. 1997, 35 (4): 907-914.PubMedPubMedCentral
5.
go back to reference Frothingham R, Meeker-O'Connell WA: Genetic diversity in the Mycobacterium tuberculosis complex based on variable numbers of tandem DNA repeats. Microbiology. 1998, 144 (Pt 5): 1189-1196. 10.1099/00221287-144-5-1189.CrossRefPubMed Frothingham R, Meeker-O'Connell WA: Genetic diversity in the Mycobacterium tuberculosis complex based on variable numbers of tandem DNA repeats. Microbiology. 1998, 144 (Pt 5): 1189-1196. 10.1099/00221287-144-5-1189.CrossRefPubMed
6.
go back to reference Le Fleche P, Fabre M, Denoeud F, Koeck JL, Vergnaud G: High resolution, on-line identification of strains from the Mycobacterium tuberculosis complex based on tandem repeat typing. BMC Microbiol. 2002, 2: 37-10.1186/1471-2180-2-37.CrossRefPubMedPubMedCentral Le Fleche P, Fabre M, Denoeud F, Koeck JL, Vergnaud G: High resolution, on-line identification of strains from the Mycobacterium tuberculosis complex based on tandem repeat typing. BMC Microbiol. 2002, 2: 37-10.1186/1471-2180-2-37.CrossRefPubMedPubMedCentral
7.
go back to reference Savine E, Warren WM, van der Spuy GD, Beyers N, van Helden PD, Locht C, Supply P: Stability of variable-number tandem repeats of mycobacterial interspersed repetitive units from 12 loci in serial isolates of Mycobacterium tuberculosis. J Clin Microbiol. 2002, 40 (12): 4561-4566. 10.1128/JCM.40.12.4561-4566.2002.CrossRefPubMedPubMedCentral Savine E, Warren WM, van der Spuy GD, Beyers N, van Helden PD, Locht C, Supply P: Stability of variable-number tandem repeats of mycobacterial interspersed repetitive units from 12 loci in serial isolates of Mycobacterium tuberculosis. J Clin Microbiol. 2002, 40 (12): 4561-4566. 10.1128/JCM.40.12.4561-4566.2002.CrossRefPubMedPubMedCentral
8.
go back to reference Supply P, Lesjean S, Savine E, Kremer K, van Soolingen D, Locht C: Automated high-throughput genotyping for study of global epidemiology of Mycobacterium tuberculosis based on mycobacterial interspersed repetitive units. J Clin Microbiol. 2001, 39 (10): 3563-3571. 10.1128/JCM.39.10.3563-3571.2001.CrossRefPubMedPubMedCentral Supply P, Lesjean S, Savine E, Kremer K, van Soolingen D, Locht C: Automated high-throughput genotyping for study of global epidemiology of Mycobacterium tuberculosis based on mycobacterial interspersed repetitive units. J Clin Microbiol. 2001, 39 (10): 3563-3571. 10.1128/JCM.39.10.3563-3571.2001.CrossRefPubMedPubMedCentral
9.
go back to reference 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 a 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): 759-772. 10.1128/JB.188.2.759-772.2006.CrossRefPubMedPubMedCentral 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 a 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): 759-772. 10.1128/JB.188.2.759-772.2006.CrossRefPubMedPubMedCentral
10.
go back to reference Gutacker MM, Mathema B, Soini H, Shashkina E, Kreiswirth BN, Graviss EA, Musser JM: Single-nucleotide polymorphism-based population genetic analysis of Mycobacterium tuberculosis strains from 4 geographic sites. J Infect Dis. 2006, 193 (1): 121-128. 10.1086/498574.CrossRefPubMed Gutacker MM, Mathema B, Soini H, Shashkina E, Kreiswirth BN, Graviss EA, Musser JM: Single-nucleotide polymorphism-based population genetic analysis of Mycobacterium tuberculosis strains from 4 geographic sites. J Infect Dis. 2006, 193 (1): 121-128. 10.1086/498574.CrossRefPubMed
11.
go back to reference de Jong BC, Antonio M, Awine T, Ogungbemi K, de Jong YP, Gagneux S, DeRiemer K, Zozio T, Rastogi N, Borgdorff M, Hill PC, Adegbola RA: Use of spoligotyping and large sequence polymorpisms to study the populations structure of Mycobacterium tuberculosis complex in a cohort study of consecutive smear-positive cases in The Gambia. J Clin Microbiol. 2009, 47 (4): 994-1001. 10.1128/JCM.01216-08.CrossRefPubMedPubMedCentral de Jong BC, Antonio M, Awine T, Ogungbemi K, de Jong YP, Gagneux S, DeRiemer K, Zozio T, Rastogi N, Borgdorff M, Hill PC, Adegbola RA: Use of spoligotyping and large sequence polymorpisms to study the populations structure of Mycobacterium tuberculosis complex in a cohort study of consecutive smear-positive cases in The Gambia. J Clin Microbiol. 2009, 47 (4): 994-1001. 10.1128/JCM.01216-08.CrossRefPubMedPubMedCentral
12.
go back to reference Flores L, Van T, Narayanan S, DeRiemer K, Kato-Maeda M, Gagneux S: Large sequence polymorphisms classify Mycobacterium tuberculosis strains with ancestral spoligotyping patterns. J Clin Microbiol. 2007, 45 (10): 3393-3395. 10.1128/JCM.00828-07.CrossRefPubMedPubMedCentral Flores L, Van T, Narayanan S, DeRiemer K, Kato-Maeda M, Gagneux S: Large sequence polymorphisms classify Mycobacterium tuberculosis strains with ancestral spoligotyping patterns. J Clin Microbiol. 2007, 45 (10): 3393-3395. 10.1128/JCM.00828-07.CrossRefPubMedPubMedCentral
13.
go back to reference Gagneux S, DeRiemer K, Van T, Kato-Maeda M, de Jong BC, Narayanan S, Nicol M, Niemann S, Kremer K, Gutierrez MC, Hilty M, Hopewell PC, Small PM: Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2006, 103 (8): 2869-2873. 10.1073/pnas.0511240103.CrossRefPubMedPubMedCentral Gagneux S, DeRiemer K, Van T, Kato-Maeda M, de Jong BC, Narayanan S, Nicol M, Niemann S, Kremer K, Gutierrez MC, Hilty M, Hopewell PC, Small PM: Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2006, 103 (8): 2869-2873. 10.1073/pnas.0511240103.CrossRefPubMedPubMedCentral
14.
go back to reference Reed MB, Pichler VK, McIntosh F, Mattia A, Fallow A, Masala S, Domenech P, Zwerling A, Thibert L, Menzies D, Schwartzman K, Behr MA: Major Mycobacterium tuberculosis lineages associate with patient country of origin. J Clin Microbiol. 2009, 47 (4): 1119-28. 10.1128/JCM.02142-08.CrossRefPubMedPubMedCentral Reed MB, Pichler VK, McIntosh F, Mattia A, Fallow A, Masala S, Domenech P, Zwerling A, Thibert L, Menzies D, Schwartzman K, Behr MA: Major Mycobacterium tuberculosis lineages associate with patient country of origin. J Clin Microbiol. 2009, 47 (4): 1119-28. 10.1128/JCM.02142-08.CrossRefPubMedPubMedCentral
15.
go back to reference Central Statistics Office: Summary Report, Zambia 2000 Census of Population and Housing. 2003, Central Statistics Office, Lusaka, Zambia Central Statistics Office: Summary Report, Zambia 2000 Census of Population and Housing. 2003, Central Statistics Office, Lusaka, Zambia
16.
go back to reference Ministry of Health: Tuberculosis and TB/HIV Manual. The National TB and Leprosy Control Programme. Ministry of Health, Lusaka, Zambia, Third Ministry of Health: Tuberculosis and TB/HIV Manual. The National TB and Leprosy Control Programme. Ministry of Health, Lusaka, Zambia, Third
17.
go back to reference World Health Organization: Treatment of tuberculosis: guidelines for national programmes. WHO/CDS/TB/2003.313. 2003, World Health Organization, Geneva, Switzerland, 3 World Health Organization: Treatment of tuberculosis: guidelines for national programmes. WHO/CDS/TB/2003.313. 2003, World Health Organization, Geneva, Switzerland, 3
18.
go back to reference Petroff SA: A new and rapid method for the isolation and cultivation of tubercle bacilli directly form the sputum and feces. J Exp Med. 1915, 21 (1): 38-42. 10.1084/jem.21.1.38.CrossRefPubMedPubMedCentral Petroff SA: A new and rapid method for the isolation and cultivation of tubercle bacilli directly form the sputum and feces. J Exp Med. 1915, 21 (1): 38-42. 10.1084/jem.21.1.38.CrossRefPubMedPubMedCentral
19.
go back to reference Supply P, Mazars E, Lesjean S, Vincent V, Gicquel B, Locht C: Variable human minisatellite-like regions in the Mycobacterium tuberculosis genome. Mol Microlbiol. 2000, 36 (3): 762-771. 10.1046/j.1365-2958.2000.01905.x.CrossRef Supply P, Mazars E, Lesjean S, Vincent V, Gicquel B, Locht C: Variable human minisatellite-like regions in the Mycobacterium tuberculosis genome. Mol Microlbiol. 2000, 36 (3): 762-771. 10.1046/j.1365-2958.2000.01905.x.CrossRef
20.
go back to reference 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 Mycobacterium tuberculosis complex isolates. J Clin Microbiol. 2008, 46 (8): 2692-2699. 10.1128/JCM.00540-08.CrossRefPubMedPubMedCentral 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 Mycobacterium tuberculosis complex isolates. J Clin Microbiol. 2008, 46 (8): 2692-2699. 10.1128/JCM.00540-08.CrossRefPubMedPubMedCentral
21.
go back to reference Shamputa IC, Rigouts L, Eyongeta LA, El Aila NA, van Deun A, Salim AH, Willery E, Locht C, Supply P, Portaels F: Genotypic and phenotypic heterogeneity among Mycobacterium tuberculosis isolates from pulmonary tuberculosis patients. J Clin Microbiol. 2004, 42 (12): 5528-5536. 10.1128/JCM.42.12.5528-5536.2004.CrossRefPubMedPubMedCentral Shamputa IC, Rigouts L, Eyongeta LA, El Aila NA, van Deun A, Salim AH, Willery E, Locht C, Supply P, Portaels F: Genotypic and phenotypic heterogeneity among Mycobacterium tuberculosis isolates from pulmonary tuberculosis patients. J Clin Microbiol. 2004, 42 (12): 5528-5536. 10.1128/JCM.42.12.5528-5536.2004.CrossRefPubMedPubMedCentral
22.
go back to reference Shamputa IC, Jugheli L, Sadradze N, Willery E, Portaels F, Supply P, Rigouts L: Mixed infection and clonal representativeness of a single sputum sample in tuberculosis patients from a penitentiary hospital in Georgia. Respir Res. 2006, 17 (7): 99-10.1186/1465-9921-7-99.CrossRef Shamputa IC, Jugheli L, Sadradze N, Willery E, Portaels F, Supply P, Rigouts L: Mixed infection and clonal representativeness of a single sputum sample in tuberculosis patients from a penitentiary hospital in Georgia. Respir Res. 2006, 17 (7): 99-10.1186/1465-9921-7-99.CrossRef
23.
go back to reference Hunter PR, Gaston MA: Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol. 1988, 26 (11): 2465-2466.PubMedPubMedCentral Hunter PR, Gaston MA: Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol. 1988, 26 (11): 2465-2466.PubMedPubMedCentral
24.
go back to reference Chihota V, Apers L, Mungofa S, Kasongo W, Nyoni IM, Tembwe R, Mbulo G, Tembo M, Streicher EM, van der Spuy GD, Victor TC, van Helden P, Warren RM: Predominance of a single genotype of Mycobacteium tuberculosis in regions of Southern Africa. Int J Tuberc Lung Dis. 2007, 11 (3): 311-318.PubMed Chihota V, Apers L, Mungofa S, Kasongo W, Nyoni IM, Tembwe R, Mbulo G, Tembo M, Streicher EM, van der Spuy GD, Victor TC, van Helden P, Warren RM: Predominance of a single genotype of Mycobacteium tuberculosis in regions of Southern Africa. Int J Tuberc Lung Dis. 2007, 11 (3): 311-318.PubMed
25.
go back to reference Easterbrook PJ, Gibson A, Murad S, Lamprecht D, Ives N, Ferguson A, Lowe O, Mason P, Ndudzo A, Taziwa A, Makombe R, Mbengeranwa L, Sola C, Rastogi N, Drobniewski F: High rates of clustering of strains causing tuberculosis in Harare, Zimbabwe: a molecular epidemiological study. J Clin Microbiol. 2004, 42 (10): 4536-4544. 10.1128/JCM.42.10.4536-4544.2004.CrossRefPubMedPubMedCentral Easterbrook PJ, Gibson A, Murad S, Lamprecht D, Ives N, Ferguson A, Lowe O, Mason P, Ndudzo A, Taziwa A, Makombe R, Mbengeranwa L, Sola C, Rastogi N, Drobniewski F: High rates of clustering of strains causing tuberculosis in Harare, Zimbabwe: a molecular epidemiological study. J Clin Microbiol. 2004, 42 (10): 4536-4544. 10.1128/JCM.42.10.4536-4544.2004.CrossRefPubMedPubMedCentral
26.
go back to reference Glynn JR, Bauer J, de Boer AS, Borgdorff MW, Fine PEM, Godfrey-Faussett P, Vynnycky E: Interpreting DNA fingerprint clusters of Mycobacterium tuberculosis. Int J Tuberc Lung Dis. 1999, 3 (12): 1055-1060.PubMed Glynn JR, Bauer J, de Boer AS, Borgdorff MW, Fine PEM, Godfrey-Faussett P, Vynnycky E: Interpreting DNA fingerprint clusters of Mycobacterium tuberculosis. Int J Tuberc Lung Dis. 1999, 3 (12): 1055-1060.PubMed
27.
go back to reference Lockman S, Sheppard JD, Braden CR, Mwasekaga MJ, Woodley CL, Kenyon TA, Binkin NJ, Steinman M, Montsho F, Kesupile-Reed M, Hirschfeldt C, Notha M, Moeti T, Tappero JW: Molecular and conventional epidemiology of Mycobacterium tuberculosis in Botswana: a population-based prospective study of 301 pulmonary tuberculosis patients. J Clin Microbiol. 2001, 39 (3): 1042-1047. 10.1128/JCM.39.3.1042-1047.2001.CrossRefPubMedPubMedCentral Lockman S, Sheppard JD, Braden CR, Mwasekaga MJ, Woodley CL, Kenyon TA, Binkin NJ, Steinman M, Montsho F, Kesupile-Reed M, Hirschfeldt C, Notha M, Moeti T, Tappero JW: Molecular and conventional epidemiology of Mycobacterium tuberculosis in Botswana: a population-based prospective study of 301 pulmonary tuberculosis patients. J Clin Microbiol. 2001, 39 (3): 1042-1047. 10.1128/JCM.39.3.1042-1047.2001.CrossRefPubMedPubMedCentral
28.
go back to reference Lockman S, Sheppard JD, Mwasekaga M, Kenyon TA, Binkin NJ, Braden CR, Woodley CL, Rumisha DW, Tappero JW: DNA fingerprinting of a national sample of Mycobacterium tuberculosis isolates, Botswana, 1995-1996. Int J Tuberc Lung Dis. 2000, 4 (6): 584-587.PubMed Lockman S, Sheppard JD, Mwasekaga M, Kenyon TA, Binkin NJ, Braden CR, Woodley CL, Rumisha DW, Tappero JW: DNA fingerprinting of a national sample of Mycobacterium tuberculosis isolates, Botswana, 1995-1996. Int J Tuberc Lung Dis. 2000, 4 (6): 584-587.PubMed
29.
go back to reference Bruchfeld J, Aderaye G, Palme IB, Bjorvatn B, Ghebremichael S, Hoffner S, Lindquist L: Molecular epidemiology and drug resistance of Mycobacterium tuberculosis isolates from Ethiopian pulmonary tuberculosis patients with and without human immunodeficiency virus infection. J Clin Microbiol. 2002, 40 (5): 1636-1643. 10.1128/JCM.40.5.1636-1643.2002.CrossRefPubMedPubMedCentral Bruchfeld J, Aderaye G, Palme IB, Bjorvatn B, Ghebremichael S, Hoffner S, Lindquist L: Molecular epidemiology and drug resistance of Mycobacterium tuberculosis isolates from Ethiopian pulmonary tuberculosis patients with and without human immunodeficiency virus infection. J Clin Microbiol. 2002, 40 (5): 1636-1643. 10.1128/JCM.40.5.1636-1643.2002.CrossRefPubMedPubMedCentral
30.
go back to reference Affolabi D, Anyo G, Faïhun F, Sanoussi N, Shamputa IC, Rigouts L, Kestens L, Anagonou S, Portaels F: First molecular epidemiological study of tuberculosis in Benin. Int J Tuberc Lung Dis. 2009, 13 (3): 317-322.PubMed Affolabi D, Anyo G, Faïhun F, Sanoussi N, Shamputa IC, Rigouts L, Kestens L, Anagonou S, Portaels F: First molecular epidemiological study of tuberculosis in Benin. Int J Tuberc Lung Dis. 2009, 13 (3): 317-322.PubMed
31.
go back to reference Crampin AC, Glynn JR, Traore H, Yates MD, Mwaungulu L, Mwenebabu M, Chaguluka SD, Floyd S, Drobniewski F, Fine PE: Tuberculosis transmission attributable to close contacts and HIV status, Malawi. Emerg Infect Dis. 2006, 12 (5): 729-735.CrossRefPubMedPubMedCentral Crampin AC, Glynn JR, Traore H, Yates MD, Mwaungulu L, Mwenebabu M, Chaguluka SD, Floyd S, Drobniewski F, Fine PE: Tuberculosis transmission attributable to close contacts and HIV status, Malawi. Emerg Infect Dis. 2006, 12 (5): 729-735.CrossRefPubMedPubMedCentral
32.
go back to reference Tostmann A, Kik SV, Kalisvaart NA, Sebek MM, Verver S, Boeree MJ, van Soolingen D: Tuberculosis transmission by patients with smear negative pulmonary tuberculosis in a large cohort in the Netherlands. Clin Infect Dis. 2008, 47 (9): 1135-1142. 10.1086/591974.CrossRefPubMed Tostmann A, Kik SV, Kalisvaart NA, Sebek MM, Verver S, Boeree MJ, van Soolingen D: Tuberculosis transmission by patients with smear negative pulmonary tuberculosis in a large cohort in the Netherlands. Clin Infect Dis. 2008, 47 (9): 1135-1142. 10.1086/591974.CrossRefPubMed
33.
go back to reference Hernandez-Garduno E, Cook V, Kunimoto D, Elwood RK, Black WA, FitzGerald JM: Transmission of tuberculosis from smear negative patients: a molecular epidemiology study. Thorax. 2004, 59 (4): 286-290. 10.1136/thx.2003.011759.CrossRefPubMedPubMedCentral Hernandez-Garduno E, Cook V, Kunimoto D, Elwood RK, Black WA, FitzGerald JM: Transmission of tuberculosis from smear negative patients: a molecular epidemiology study. Thorax. 2004, 59 (4): 286-290. 10.1136/thx.2003.011759.CrossRefPubMedPubMedCentral
34.
go back to reference Lawn SD, Edwards D, Wood R: Tuberculosis transmission from patients with smear negative pulmonary tuberculosis in sub-Saharan Africa. Clin Infect Dis. 2009, 48 (4): 496-497. 10.1086/596550.CrossRefPubMedPubMedCentral Lawn SD, Edwards D, Wood R: Tuberculosis transmission from patients with smear negative pulmonary tuberculosis in sub-Saharan Africa. Clin Infect Dis. 2009, 48 (4): 496-497. 10.1086/596550.CrossRefPubMedPubMedCentral
35.
go back to reference Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-Gerdes S, Willery E, Savine E, de Haas P, van Deutekom H, Roring S, Bifani P, Kurepina N, Kreiswirth B, Sola C, Rastogi N, Vatin V, Gutierrez MC, Fauville M, Niemann S, Skuce R, Kremer K, Locht L, van Soolingen D: Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2006, 44 (12): 4498-4510. 10.1128/JCM.01392-06.CrossRefPubMedPubMedCentral Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-Gerdes S, Willery E, Savine E, de Haas P, van Deutekom H, Roring S, Bifani P, Kurepina N, Kreiswirth B, Sola C, Rastogi N, Vatin V, Gutierrez MC, Fauville M, Niemann S, Skuce R, Kremer K, Locht L, van Soolingen D: Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2006, 44 (12): 4498-4510. 10.1128/JCM.01392-06.CrossRefPubMedPubMedCentral
36.
go back to reference Stavrum R, Mphahlele M, Ovreås K, Muthivhi T, Fourie PB, Weyer K, Grewal HM: High diversity of Mycobacterium tuberculosis genotypes in South Africa and preponderance of mixed infections among ST53 isolates. J Clin Microbiol. 2009, 47 (6): 1848-1856. 10.1128/JCM.02167-08.CrossRefPubMedPubMedCentral Stavrum R, Mphahlele M, Ovreås K, Muthivhi T, Fourie PB, Weyer K, Grewal HM: High diversity of Mycobacterium tuberculosis genotypes in South Africa and preponderance of mixed infections among ST53 isolates. J Clin Microbiol. 2009, 47 (6): 1848-1856. 10.1128/JCM.02167-08.CrossRefPubMedPubMedCentral
37.
go back to reference Shamputa IC, Lee J, Allix-Béguec C, Cho E, Lee J, Rajan V, Lee EG, Min JH, Carroll MW, Goldfeder LC, Kim JH, Kang HS, Hwang S, Eum S, Park SK, Lee H, Supply P, Cho SN, Via LE, Barry CE: Genetic diversity of Mycobacterium tuberculosis isolates from a tertiary tuberculosis hospital in South Korea. J Clin Microbiol. 2010, 48 (2): 387-394. 10.1128/JCM.02167-09.CrossRefPubMed Shamputa IC, Lee J, Allix-Béguec C, Cho E, Lee J, Rajan V, Lee EG, Min JH, Carroll MW, Goldfeder LC, Kim JH, Kang HS, Hwang S, Eum S, Park SK, Lee H, Supply P, Cho SN, Via LE, Barry CE: Genetic diversity of Mycobacterium tuberculosis isolates from a tertiary tuberculosis hospital in South Korea. J Clin Microbiol. 2010, 48 (2): 387-394. 10.1128/JCM.02167-09.CrossRefPubMed
38.
go back to reference Warren RM, Victor TC, Streicher EM, Richardson M, Beyers N, Gey van Pittius NC, van Helden PD: Patients with active tuberculosis often have different strains in the same sputum specimen. Am J Respir Crit Care Med. 2004, 169 (5): 610-614. 10.1164/rccm.200305-714OC.CrossRefPubMed Warren RM, Victor TC, Streicher EM, Richardson M, Beyers N, Gey van Pittius NC, van Helden PD: Patients with active tuberculosis often have different strains in the same sputum specimen. Am J Respir Crit Care Med. 2004, 169 (5): 610-614. 10.1164/rccm.200305-714OC.CrossRefPubMed
Metadata
Title
Diversity of Mycobacterium tuberculosis genotypes circulating in Ndola, Zambia
Authors
Chanda Mulenga
Isdore C Shamputa
David Mwakazanga
Nathan Kapata
Françoise Portaels
Leen Rigouts
Publication date
01-12-2010
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2010
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-10-177

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