Multidrug-resistant Tuberculosis Control in Rwanda Overcomes a Successful Clone that Causes Most Disease over a Quarter Century

Journal Articles
, Tuberculosis

Multidrug-resistant Tuberculosis Control in Rwanda Overcomes a Successful Clone that Causes Most Disease over a Quarter Century

By: Jean Claude S Ngabonziza, Leen Rigouts, Gabriela Torrea, Tom Decroo, Eliane Kamanzi, Pauline Lempens, Aniceth Rucogoza, Yves M Habimana, Lies Laenen, Belamo E Niyigena, Cécile Uwizeye, Bertin Ushizimpumu, Wim Mulders, Emil Ivan, Oren Tzfadia, Claude Mambo Muvunyi, Patrick Migambi, Emmanuel Andre, Jean Baptiste Mazarati, Dissou Affolabi, Alaine N Umubyeyi, Sabin Nsanzimana, Françoise Portaels, Michel Gasana, Bouke C de Jong, Conor J Meehan

Publication: Journal of Clinical Tuberculosis and Other Mycobacterial Diseases; 24 Jan. 2022; 27:100299. DOI: 10.1016/j.jctube.2022.100299

Abstract

Multidrug-resistant (MDR) tuberculosis (TB) poses an important challenge in TB management and control. Rifampicin resistance (RR) is a solid surrogate marker of MDR-TB. We investigated the RR-TB clustering rates, bacterial population dynamics to infer transmission dynamics, and the impact of changes to patient management on these dynamics over 27 years in Rwanda. 

Results: Of 308 baseline RR-TB isolates considered for transmission analysis, the clustering analysis grouped 259 (84.1%) isolates into 13 clusters. Within these clusters, a single dominant clone was discovered containing 213 isolates (82.2% of clustered and 69.1% of all RR-TB), which we named the “Rwanda Rifampicin-Resistant clone” (R3clone). R3clone isolates belonged to Ugandan sub-lineage 4.6.1.2 and its rifampicin and isoniazid resistance were conferred by the Ser450Leu mutation in rpoB and Ser315Thr in katG genes, respectively. All R3clone isolates had Pro481Thr, a putative compensatory mutation in the rpoC gene that likely restored its fitness. The R3clone was estimated to first arise in 1987 and its population size increased exponentially through the 1990s’, reaching maximum size (∼84%) in early 2000 s’, with a declining trend since 2014. Indeed, the highest proportion of R3clone (129/157; 82·2%, 95%CI: 75·3-87·8%) occurred between 2000 and 13, declining to 64·4% (95%CI: 55·1-73·0%) from 2014 onward. We showed that patients with R3clone detected after an unsuccessful category 2 treatment were more likely to generate secondary cases than patients with R3clone detected after an unsuccessful category 1 treatment regimen. 

Conclusions: RR-TB in Rwanda is largely transmitted. Xpert MTB/RIF assay as first diagnostic test avoids unnecessary rounds of rifampicin-based TB treatment, thus preventing ongoing transmission of the dominant R3clone. As PMDT was intensified and all TB patients accessed rifampicin-resistance testing, the nationwide R3clone burden declined. To our knowledge, our findings provide the first evidence supporting the impact of universal DST on the transmission of RR-TB.