Strain variation and anomalous climate synergistically influence cholera pandemics

PLoS Negl Trop Dis. 2024 Aug 1;18(8):e0012275. doi: 10.1371/journal.pntd.0012275. eCollection 2024 Aug.

Abstract

Background: Explanations for the genesis and propagation of cholera pandemics since 1817 have remained elusive. Evolutionary pathogen change is presumed to have been a dominant factor behind the 7th "El Tor" pandemic, but little is known to support this hypothesis for preceding pandemics. The role of anomalous climate in facilitating strain replacements has never been assessed. The question is of relevance to guide the understanding of infectious disease emergence today and in the context of climate change.

Methodology/principal findings: We investigate the roles of climate and putative strain variation for the 6th cholera pandemic (1899-1923) using newly assembled historical records for climate variables and cholera deaths in provinces of former British India. We compare this historical pandemic with the 7th (El Tor) one and with the temporary emergence of the O139 strain in Bangladesh and globally. With statistical methods for nonlinear time series analysis, we examine the regional synchrony of outbreaks and associations of the disease with regional temperature and rainfall, and with the El Niño Southern Oscillation (ENSO). To establish future expectations and evaluate climate anomalies accompanying historical strain replacements, climate projections are generated with multi-model climate simulations for different 50-year periods. The 6th cholera pandemic featured the striking synchronisation of cholera outbreaks over Bengal during the El Niño event of 1904-07, following the invasion of the Bombay Presidency with a delay of a few years. Accompanying anomalous weather conditions are similar to those related to ENSO during strain replacements and pandemic expansions into Africa and South America in the late 20th century. Rainfall anomalies of 1904-05 at the beginning of the large cholera anomaly fall in the 99th percentile of simulated changes for the regional climate.

Conclusions/significance: Evolutionary pathogen change can act synergistically with climatic conditions in the emergence and propagation of cholera strains. Increased climate variability and extremes under global warming provide windows of opportunity for emerging pathogens.

Publication types

  • Historical Article

MeSH terms

  • Bangladesh / epidemiology
  • Cholera* / epidemiology
  • Climate
  • Climate Change
  • History, 19th Century
  • History, 20th Century
  • Humans
  • India / epidemiology
  • Pandemics*
  • Vibrio cholerae / genetics

Grants and funding

We thank the Indian Institute for Tropical Meteorology at Pune (http://www.tropmet.res.in) for supplying meteorological data and the early support for our cholera work by NSF-NIH (Ecology of Infectious Diseases Program, NSF 0545276 and 0430120) and NOAA (Oceans and Health, NA040AR460019) to M.P. X.R acknowledges the support of the PERIS-PICAT project of the Catalan Dep. Salut and PARA-CLIM-CHANDIRGARGH of the New Indigo EU-India program. We acknowledge support from the Spanish Ministry of Science and Innovation through the “Centro de Excelencia Severo Ochoa 2019–2023” Program (CEX2018-000806-S), and support from the Generalitat de Catalunya through the CERCA Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.