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Journal of Clinical Microbiology, October 2004, p. 4536-4544, Vol. 42, No. 10
0095-1137/04/$08.00+0     DOI: 10.1128/JCM.42.10.4536-4544.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

High Rates of Clustering of Strains Causing Tuberculosis in Harare, Zimbabwe: a Molecular Epidemiological Study

Philippa J. Easterbrook,1* Andrea Gibson,2 Shahed Murad,1 Dianie Lamprecht,2 Natalie Ives,1 Alex Ferguson,3 Odette Lowe,4 Peter Mason,3 Angelika Ndudzo,3 Alfred Taziwa,3 Robert Makombe,5 Lovemore Mbengeranwa,5 Christophe Sola,6 Nalim Rostogi,6 and Francis Drobniewski2

Department of HIV/GUM, The Guy's, King's and St. Thomas' School of Medicine, King's College Hospital, Denmark Hill Campus,1 Health Protection Agency, Mycobacterial Reference Unit, Guy's, King's and St. Thomas' School of Medicine, King's College Hospital (Dulwich), London, United Kingdom,2 University of Zimbabwe,3 Harare City Health Department, Harare,5 National TB Reference Laboratory, Bulawayo, Zimbabwe,4 Institute Pasteur, Pointe à Pitre, Guadeloupe6

Received 13 November 2003/ Returned for modification 5 February 2004/ Accepted 18 June 2004

We examined the pattern of tuberculosis (TB) transmission (i.e., reactivation versus recent transmission) and the impact of human immunodeficiency virus (HIV) infection in Harare, Zimbabwe. Consecutive adult smear-positive pulmonary TB patients presenting to an urban hospital in Harare were enrolled. A detailed epidemiological questionnaire was completed, and tests for HIV type 1 and CD4 cell counts were performed for each patient. Molecular fingerprinting of the genomic DNA recovered from cultures of sputum was performed by two molecular typing methods: spacer oligonucleotide typing (spoligotyping) and analysis of variable number of tandem DNA repeats (VNTRs). A cluster was defined as isolates from two or more patients that shared the same spoligotype pattern or the same VNTR pattern, or both. DNA suitable for typing was recovered from 224 patients. The prevalence of HIV infection was 79%. Of 187 patient isolates (78.6%) typed by both spoligotyping and analysis of VNTRs, 147 were identified as part of a cluster by both methods. By spoligotyping alone, 84.1% of patient isolates were grouped into 20 clusters. The cluster size was generally <8 patient isolates, although three large clusters comprised 68, 25, and 23 patient isolates. A total of 89.4% of the patient isolates grouped into 12 clusters defined by analysis of VNTRs, with 2 large clusters consisting of 127 and 13 patient isolates, respectively. Thirty-six percent of patient isolates with a shared spoligotype and 17% with a shared VNTR pattern were geographically linked within Harare, but they were not linked on the basis of the patient's home district. In a multivariate analysis, there were no independent predictors of clustering, including HIV infection status. Comparison with the International Spoligotype database (Pasteur Institute, Pointe à Pitre, Guadeloupe) demonstrated that our three largest spoligotype clusters are well recognized and ubiquitous in Africa. In this epidemiologically well characterized urban population with a high prevalence of HIV infection, we identified a very high level of strain clustering, indicating substantial ongoing recent TB transmission. Geographic linkage could be detected in a proportion of these clusters. A small group of actively circulating strains accounted for most of the cases of TB transmission.

* Corresponding author. Mailing address: Department of HIV/GU Medicine, The Guy's, King's and St. Thomas's School of Medicine, Weston Education Centre, Cutcombe Rd., King's College Hospital, Denmark Hill Campus, London SE5 9RT, United Kingdom. Phone: 020 7848 5770. Fax: 020 7848 5769. E-mail: philippa.easterbrook{at}kcl.ac.uk.

Journal of Clinical Microbiology, October 2004, p. 4536-4544, Vol. 42, No. 10
0095-1137/04/$08.00+0     DOI: 10.1128/JCM.42.10.4536-4544.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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