Historical and genomic data reveal the influencing factors on global transmission velocity of plague during the Third Pandemic

Abstract

Quantitative knowledge about which natural and anthropogenic factors influence the global spread of plague remains sparse. We estimated the worldwide spreading velocity of plague during the Third Pandemic, using more than 200 years of extensive human plague case records and genomic data, and analyzed the association of spatiotemporal environmental factors with spreading velocity. Here, we show that two lineages, 2.MED and 1.ORI3, spread significantly faster than others, possibly reflecting differences among strains in transmission mechanisms and virulence. Plague spread fastest in regions with low population density and high proportion of pasture- or forestland, findings that should be taken into account for effective plague monitoring and control. Temperature exhibited a nonlinear, U-shaped association with spread speed, with a minimum around 20 °C, while precipitation showed a positive association. Our results suggest that global warming may accelerate plague spread in warm, tropical regions and that the projected increased precipitation in the Northern Hemisphere may increase plague spread in relevant regions.

Plague risk in the western United States over seven decades of environmental change

“…Its apparent association with colder locations in the United States may therefore not be directly related to some temperature threshold, but possibly to the ecological niche of key maintenance hosts or key vector species. For human plague risk, we see a sharp increase as the mean and maximum annual temperature falls between 5° and 14°, respectively, matching previous findings from empirical work on North American fleas 73,74 and global models of the Third Pandemic spread 75 . This may reflect the underlying thermal ecology of the pathogen 72 , or potentially some combination of rodent habitat and human behavior (e.g., these thresholds might delineate the general type of wilderness areas in the Rocky Mountains where people live alongside plague reservoirs).…”

Climate drivers of plague epidemiology in British India, 1898–1949

“…We did not find this in our data. This was in contrast to a study by Xu et al [27], demonstrating high speeds of plague spread globally during the third plague pandemic influenced by temperature. Our findings may be attributable to temperature and rainfall gradients being fairly flat across most of the Indian Peninsula (in terms of magnitude and timing), so it was unlikely that temperature or rainfall played decisive roles in dictating plague outbreaks in British India during the third pandemic.…”

“…High rainfall can flood rodent burrows, driving them towards urban areas [21] and low resources during winter can reduce rodent populations [22]. Combining these factors can have drastic effects on plague epidemiology [23][24][25]; climate drivers can facilitate the introduction of bacteria into naive rodent populations [26,27], from which plague outbreaks can emerge annually within human populations [9,28].…”

Biovar-related differences apparent in the flea foregut colonization phenotype of distinct Yersinia pestis strains do not impact transmission efficiency

“…Recent phylogenetic analyses provide enhanced resolution of Y. pestis strain characteristics, evolutionary history of biovars and associated lineages, strain geographical pattern distinctiveness, and plague spread [10,11]. Additionally, mathematical modelling reveals that branch 1 Orientalis and branch 2 Medievalis lineage strains spread significantly faster than others [12][13][14][15].…”

“…Use of the CO92 strain was motivated by several factors. First, CO92 belongs to the Orientalis branch 1 lineage comprising globally circulating strains, some directly implicated in causing the highest contemporary plague global case burden [12,26,27]. In contrast, Antiqua and Medievalis bvs are typically associated with enzootic rodent species in long term plague foci in Africa and Asia [28].…”