Dynamics of cholera epidemics from Benin to Mauritania

Abstract

Background: The countries of West Africa are largely portrayed as cholera endemic, although the dynamics of outbreaks in this region of Africa remain largely unclear.

Methodology/principal findings: To understand the dynamics of cholera in a major portion of West Africa, we analyzed cholera epidemics from 2009 to 2015 from Benin to Mauritania. We conducted a series of field visits as well as multilocus variable tandem repeat analysis and whole-genome sequencing analysis of V. cholerae isolates throughout the study region. During this period, Ghana accounted for 52% of the reported cases in the entire study region (coastal countries from Benin to Mauritania). From 2009 to 2015, we found that one major wave of cholera outbreaks spread from Accra in 2011 northwestward to Sierra Leone and Guinea in 2012. Molecular epidemiology analysis confirmed that the 2011 Ghanaian isolates were related to those that seeded the 2012 epidemics in Guinea and Sierra Leone. Interestingly, we found that many countries deemed "cholera endemic" actually suffered very few outbreaks, with multi-year lulls.

Conclusions/significance: This study provides the first cohesive vision of the dynamics of cholera epidemics in a major portion of West Africa. This epidemiological overview shows that from 2009 to 2015, at least 54% of reported cases concerned populations living in the three urban areas of Accra, Freetown, and Conakry. These findings may serve as a guide to better target cholera prevention and control efforts in the identified cholera hotspots in West Africa.

Fig 1. Weekly evolution of cholera epidemics, rainfall levels, and the tested V. cholerae isolates in Greater Accra Region from 2011 to 2014.

Suspected cholera cases are indicated in red (right y-axis), and rainfall is indicated in blue (left y-axis). The corresponding year is labeled on the x-axis. To integrate the epidemiological and MLVA/MST data, the three major MST clusters identified in Accra are indicated below the histogram of suspected cholera cases. GAR1 = the Ghana 2011 cluster (which gave rise to a few strains in 2012), GAR2 = the main Ghana 2012 cluster, and GAR3 = the Ghana 2014 cluster identified on the MST.

Fig 2. Distribution of cholera cases during the initial six weeks of epidemic escalation in Accra Metropolis from 2011 to 2014.

The cumulative cases reported in the Accra Metropolis line list for each neighborhood during the first six weeks of each epidemic are indicated with red circles. Circle size represents the relative number of cases reported in each neighborhood. The neighborhoods of Maamobi, Nima, Accra New Town, and Adabraka often reported many cases during the first six weeks of each outbreak. Many parts of Ablekuma reported several cholera cases during outbreak onset. Labadi was the hardest-hit zone during the beginning of the 2014 epidemic. In contrast, certain nearby residential areas remained largely cholera-free (e.g., Dzorwulu and Roman Ridge), despite major outbreaks in adjacent neighborhoods. The total cases accounted for and percentage coverage of sites localized for each epidemic are as follows: 2011 (897 cases; 88%), first 2012 epidemic (780 cases; 92%), second 2012 epidemic (932 cases; 94%), and 2014 (913 cases; 86%). The districts adjacent to Accra Metropolis are grayed out. Abbreviations: ANT/A, Accra New Town; Mbi, Maamobi; Adbk, Adabraka; La, Labadi; Nm, Nima.

Fig 3. Minimum Spanning Tree based on the MLVA types of 257 V. cholerae isolates from several recent West African cholera outbreaks.

Each MLVA type is represented by a node (and a unique number), and the size of the nodes reflects the number of isolates of each MLVA type. The solid lines indicate the most likely single locus variant, while dashed lines indicate the most likely double locus variant. The colors reflect the distinct country and year of isolate origin. Pie charts indicate strains from different time periods or countries displaying an identical MLVA type. The two strains represented by MLVA types #1 and #44 were isolated from environmental samples in Guinea (encircled in red). Labels A through G indicate the isolates from Ghana, Togo, and Guinea included on the phylogenic tree in Fig 4.

Fig 4. Strains from Ghana, Togo, and Guinea situated on the maximum likelihood phylogenetic tree of the third wave of the seventh pandemic lineage of V. cholerae.

The tree is based on the SNP differences across the whole core genome. An isolate from the first wave, Bangladesh 1975, was included as an outgroup to root the tree. An isolate from the second wave was also included (India 1990). The color of the branch tips indicates the country of origin, and the year of isolation is specified. The strains from Ghana, Togo, and Guinea are indicated using the same colors as in the Minimum Spanning Tree (Ghana in pink and red, Togo in orange and yellow, and Guinea in bright green). Labels A through G indicate the isolates from Ghana, Togo, and Guinea included on the MST in Fig 3. Scale is provided as the number of substitutions per variable site, and the SNPs are indicated on the branches.