Human ectoparasites and the spread of plague in Europe during the Second Pandemic

Image: Global distribution of natural plague foci, March 2016.

Plague is a disease that is known for three large pandemics in recent human history; the First Pandemic (6th-8th century Europe and the Middle East, starting with Justinian’s Plague in 541AD), the Second Pandemic (14th-19th century Europe, Northern Africa, the Middle East and Central Asia, starting with the Black Death in 1346), and the Third Pandemic (late 18th-20th century, worldwide). The disease is still widespread today in wildlife rodent populations, especially in the semi-arid deserts and alpine meadows of Central Asia, and in the western United States. In an earlier publication, we looked at the connection between the plague foci of Central Asia, and potential re-introductions of plague into Europe during the second plague pandemic.

In the 19th century, during the time of the Third Pandemic, the cause of plague was discovered to be the bacterium we now call Yersinia pestis, and much of our knowledge about plague, such as the important role of the black rat (Rattus rattus) came from studying outbreaks during that time. That understanding was later on used to try and understand the first two pandemics better.

Yet there are remarkable differences between the pandemics that cannot easily be explained by assuming that the first two pandemics were caused by a similar process as observed in the Third Pandemic. Foremost, the death toll of the initial outbreaks in the first two epidemics was a staggering 30–60% (DeWitte & Kowaleski, 2017) of the population, whereas the Third Pandemic was comparatively mild (, history of plague).

One possible explanation is that plague spread in a different way in the past than it did in the Third Pandemic. From the Third Pandemic, we know that plague can spread rapidly through rat populations, and as the rat population gets depleted their fleas start seeking out other hosts including humans. However, there are alternative routes through which plague can spread without rats. Plague can spread through droplets in the air, as recently witnessed in Madagascar, and is then called pneumonic plague. The disease is also hypothesized to spread from human to human, with ectoparasites like the human flea or body lice as a vector (Hufthammer & Walløe 2013).

Our current paper, published in the journal PNAS, is the work of my PhD student Katie R. Dean. She focused on finding out the dominant way in which plague was transmitted within cities during the Second plague pandemic in Europe. We collected high-resolution mortality data from nine historical outbreaks and three modern outbreaks, and tested this dataset on a human ectoparasite model of plague transmission, namely body lice and human fleas, as well as on conventional models for rat-borne and pneumonic plague transmission.

Summary of the mortality records used, and the comparative fit (by delta BIC) of the three transmission models tested. EP = human ectoparasite, PP = primary pneumonic, and RP = rat–flea plague.

We found that in 7 out of 9 cities, the human ectoparasite model best matched the shape of the mortality curves of plague outbreaks in cities during the Second Pandemic. For the 2 smallest outbreaks, where there is more uncertainty in all models, the human ectoparasite model was once tied with the rat-borne and once tied with the pneumonic plague model (in technical terms, a ΔBIC<10).

Fit of three models of plague transmission for the first three of nine cities (see PNAS for complete figure). Each of the three models was allowed to converge to the best possible fit it could achieve, given the structure of the model and biologically plausible parameter ranges to explore

Until now, the hypothesis of human ectoparasite transmission has been regarded as highly speculative and was supported only by indirect evidence, like different overall mortality levels between the Second and Third Pandemics, the scarcity of rat bones in archeological digs, and the presence of ancient DNA from louse-borne diseases in a plague victim (Leulmi et al, 2014). While modeling studies are not necessarily decisive, they do offer powerful insights into disease processes where experimental, historical, and archaeological information is lacking, and can serve as a stepping stone for other disciplines to build upon. With our results, we hope to shift some attention away from the rat transmission paradigm and open up new avenues for research (experimental, epidemiological and historical) into human ectoparasites as important vectors in past and current plague epidemics.

Where to next from here? Worldwide there are historians and scientists working on plague, and new, exciting findings are made regularly. The plague group at CEES — the Centre for Ecological and Evolutionary Synthesis, is focused on connecting the ecology and climate-sensitivity of plague to the information that comes from ancient plague DNA recovered from plague victims, the evolution of plague within its natural foci, and applying quantitative biology to historical records of plague outbreaks (some of the past papers here). Hope to share more with you soon!

EU grant: ERC MedPlag 324249

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