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The Epidemiology of Plague in Europe: Inferring Transmission Dynamics from Historical Data

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The Epidemiology of Plague in Europe: Inferring Transmission Dynamics from Historical Data The epidemiology of plague in Europe: inferring transmission dynamics from historical data Katharine R. Dean Dissertation presented for a degree of Philosophiae Doctor (PhD) 2019 Centre for Ecological and Evolutionary Synthesis Department of Biosciences Faculty of Mathematics and Natural Sciences University of Oslo © Katharine R. Dean, 2019 Series of dissertations submitted to the Faculty of Mathematics and Natural Sciences, University of Oslo No. 2160 ISSN 1501-7710 All rights reserved. No part of this publication may be reproduced or transmitted, in any form or by any means, without permission. Cover: Hanne Baadsgaard Utigard. Print production: Reprosentralen, University of Oslo. Acknowledgments My PhD has been an unforgettable experience, filled with laughter, triumphs, setbacks, and a few adventures. My utmost thanks to my supervisors Boris Schmid, Nils Chr. Stenseth, and Hildegunn Viljugrein, for giving me the support and freedom to pursue new ideas. I am continually grateful for your optimism, curiosity, and willingness to send me just about anywhere for a conference. I would also like to thank my co-authors for their contributions to the papers in this thesis. I would certainly not be doing a PhD without the financial and moral support of MedPlag and CEES. I would especially like to thank Barbara who has always championed my work, even though it has nothing to do with ancient DNA. It has been a pleasure to be part of MedPlag: Fabienne, Pernille, Meriam, Claudio, Oliver, Amine, Ryan, Thomas, Lars, and Lei—thanks for always giving the best advice and for making days at the office a little brighter. Working at CEES over the last few years has been an absolute pleasure and I am eternally grateful for my friends at work for sharing coffee breaks, lunches, stories, knitting, cheese, and running. I am so lucky to have my family and friends in the United States and abroad, who have forgiven me (a few times) for moving far away. To my parents, thank you for encouraging me to pursue all of life’s adventures. To my brother, thanks for taking custody of our cats, Lemon and Hexa, and for upgrading my computational resources along the way. To Katie S., Kate M., Annie, and Laura, thanks for weekend trips, care packages, skype dates, and for simply always picking up where we left off. Finally, my world and this acknowledgement would not be complete without Martin and James, who fill my days with happiness even when I insist on being tired and grumpy. Ta bl e o f C o n te n t s Acknowledgments ................................................................................................................... i List of papers ........................................................................................................................... 1 Summary .................................................................................................................................. 3 Introduction............................................................................................................................. 5 Ecology ................................................................................................................................. 5 Transmission ....................................................................................................................... 7 Epidemiology and Clinical forms .................................................................................. 10 Bubonic plague ............................................................................................................. 11 Pneumonic plague ....................................................................................................... 12 Septicemic plague ........................................................................................................ 13 History of plague ............................................................................................................. 13 First pandemic ............................................................................................................. 14 Second pandemic ........................................................................................................ 15 Third pandemic............................................................................................................ 18 Aims ....................................................................................................................................... 20 Approaches ........................................................................................................................... 21 Paper Summaries ................................................................................................................. 23 Paper I. Human ectoparasites and the spread of plague in Europe during the Second Pandemic ............................................................................................................ 23 Paper II. Epidemiology of a bubonic plague outbreak in Glasgow, Scotland in 1900 ............................................................................................................................................ 23 Paper III. The third plague pandemic in Europe ....................................................... 24 Discussion ............................................................................................................................. 25 Mechanisms of plague transmission in Europe ......................................................... 25 Characteristics of European plague epidemics ......................................................... 26 The decline of plague in Europe .................................................................................. 28 Challenges of using historical data............................................................................... 28 Conclusions and future perspectives .......................................................................... 29 References ............................................................................................................................ 31 iii List of papers Paper I. Human ectoparasites and the spread of plague in Europe during the Second Pandemic Katharine R. Dean, Fabienne Krauer, Lars Walløe, Ole Christian Lingjærde, Barbara Bramanti, Nils Chr. Stenseth, and Boris V. Schmid Proceedings of the National Academy of Sciences USA, doi: 10.1073/pnas.1715640115 Paper II. Epidemiology of a bubonic plague outbreak in Glasgow, Scotland in 1900 Katharine R. Dean, Fabienne Krauer, and Boris V. Schmid Royal Society Open Science, doi: 10.1098/rsos.181695 Paper III. The third plague pandemic in Europe Barbara Bramanti*, Katharine R. Dean*, Lars Walløe, and Nils Chr. Stenseth *These authors contributed equally Proceedings of the Royal Society B, doi: 10.1098/rspb.2018.2429 (in press) 1 Summary Throughout history, plague (Yersinia pestis) has caused devastating outbreaks in human populations around the world, however, the mechanisms that have given rise to plague epidemics are still poorly understood. With an emphasis on transmission, this thesis investigates the epidemiology of plague outbreaks in Europe using quantitative methods. Several hypotheses have been proposed to explain the rapid spread of plague in Europe during the Black Death and throughout the Second Pandemic. The first paper in this thesis develops a novel mechanistic model for plague transmission by human ectoparasites, namely body lice and human fleas. By fitting the model to historical mortality data using Markov Chain Monte Carlo simulations in a Bayesian framework and comparing it to other candidate models, we demonstrate that human ectoparasite transmission could explain the development of large plague epidemics under certain conditions. A challenge of modeling historical plague epidemics is that there are very few studies which have estimated parameters for untreated plague cases. In the second paper, we provide a detailed analysis of plague in the pre-antibiotic era using an outbreak from Glasgow, Scotland in 1900 as a case-study. Using a machine learning method (Expectation-Maximization), we reconstruct the transmission network for the outbreak from clinical and contact-tracing records. We provide estimates for several epidemiological parameters for bubonic plague, most likely spread between humans, possibly through a human ectoparasite vector. Although often overlooked, plague outbreaks in Europe during the Third Pandemic may be used to better understand those during the Second Pandemic. In the third paper, we compile reports of internationally notified plague cases in Europe during the Third Pandemic. We show that there were more than 1,600 suspected cases of plague in Europe between 1899 and 1950. We found that most of these cases were distributed in coastal and inland ports, suggesting that the main source of 3 plague was from maritime shipping, not a local reservoir. Furthermore, we highlight the international efforts used to prevent the spread of infectious diseases and the improved hygienic conditions in Europe, which ultimately led to disappearance of plague. In conclusion, this thesis improves our understanding of the mechanisms underlying the spread of plague in Europe using epidemiological models and historical outbreak records. 4 Introduction Plague is a vector-borne zoonotic disease caused by the gram-negative bacterium Yersinia pestis, which primarily affects rodents. Y. pestis is maintained in a natural cycle, driven by transmission between rodent hosts and flea
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