Abstract

Identifying key reservoirs for zoonoses is crucial for understanding variation in incidence. Plague re-emerged in Mahajanga, Madagascar in the 1990s but there has been no confirmed case since 1999. Here we combine ecological and genetic data, from during and after the epidemics, with experimental infections to examine the role of the shrew Suncus murinus in the plague epidemiological cycle. The predominance of S. murinus captures during the epidemics, their carriage of the flea vector and their infection with Yersinia pestis suggest they played an important role in the maintenance and transmission of plague. S. murinus exhibit a high but variable resistance to experimental Y. pestis infections, providing evidence of its ability to act as a maintenance host. Genetic analyses of the strains isolated from various hosts were consistent with two partially-linked transmission cycles, with plague persisting within the S. murinus population, occasionally spilling over into the rat and human populations. The recent isolation from a rat in Mahajanga of a Y. pestis strain genetically close to shrew strains obtained during the epidemics reinforces this hypothesis and suggests circulation of plague continues. The observed decline in S. murinus and Xenopsylla cheopis since the epidemics appears to have decreased the frequency of spillover events to the more susceptible rats, which act as a source of infection for humans. Although this may explain the lack of confirmed human cases in recent years, the current circulation of plague within the city highlights the continuing health threat.

Highlights

  • Plague, like other zoonoses, can exhibit large temporal variation in incidence at the same location, sometimes re-emerging after long periods of silence or apparently disappearing

  • Using data and samples collected during and immediately after the epidemics in 1990s and recently (2011–2014), this study examines the role of S. murinus in maintaining the plague focus and as a source of the human epidemics by (i) comparing seasonal and inter-annual changes in reservoir host and flea abundance and seroprevalence of antibodies to plague amongst reservoir hosts; (ii) comparing sensitivity of current populations of potential reservoir hosts to two Y. pestis strains isolated from R. norvegicus and S. murinus during the epidemics; and (iii) conducting genetic analyses on whole genome sequences of Y. pestis isolates from Mahajanga

  • Our study investigated the seasonal abundance of reservoirs and vectors for plague in Mahajanga, the dynamics of the antibody response in shrews and rats, the susceptibility of shrews to plague and the genetic relationship between Y. pestis strains isolated from humans, rats, shrews and fleas

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Summary

Introduction

Like other zoonoses, can exhibit large temporal variation in incidence at the same location, sometimes re-emerging after long periods of silence or apparently disappearing. Such variation in exposure may be due to changes in the presence or prevalence of the pathogen within the reservoir community or in the contact between humans and infected reservoirs (or vectors). Between August 1991 and April 1992, plague reappeared after more than 60 years of silence in Mahajanga, a city on the north-west coast of Madagascar with 202 suspected cases including 41 probable and confirmed human cases [4,5,6], after recolonization by a strain originating from the Central Highlands foci [7,8]. From a public health viewpoint it is important to understand the role of different reservoir hosts in allowing plague to re-emerge in Mahajanga in the 1990s and whether plague persists today

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