conceived the work; B.B., L.W. Ancient DNA studies have identified Yersinia pestis, the aetiological agent of the Third Pandemic, as the cause of the previous plague pandemics: the First Pandemic (sixth to eighth centuries) [1–3] and the Second Pandemic (fourteen to nineteenth centuries) [4–8]. The local authorities concluded that the infected rats were most probably brought by grain ships which unloaded their cargo in the area to lighten their draught before continuing onwards [36,44]. Europe is also the only region for which we have extended records and accounts on the previous plague pandemics, in particular those of the Second Pandemic. In 1945, they found only two rats tested positive  and, in 1946, none were infected . The Third Pandemic of 1894 . In addition to rats, the authorities found some ferrets, cats and rabbits that died of plague . Thus, having documented outbreaks of the Third Pandemic can enable comparisons with historical ones, especially considering that the Third Pandemic in Europe was restricted to the pre-antibiotic era. In addition, from the middle of the twentieth century, the number of pests and parasites was reduced by the introduction of insecticides like dichlorodiphenyltrichloroethane (DDT), which was used heavily in many places like Malta from 1946 onwards . The earliest recorded pandemic happened during the Peloponnesian War. For some of the early outbreaks, such as those in Porto (1899) and Glasgow (1900), the cases are more temporally resolved. Some regions, such as the Nordics and Eastern Europe, did not report any case of plague. Plague has a long history on the European continent, with evidence of the disease dating back to the Stone Age. The prevailing view among researchers in the Indo-Pacific region, including Thompson  who observed plague outbreaks in Sydney, Hunter who reported on plague in Hong Kong  and those of the Indian Plague Commission , was that black rats played an important role in the spread of plague, both as hosts in the chain of transmission and as carriers of the disease on ships . Indeed, in the last years, the frequency of plague outbreaks in developing countries in Africa should not be overlooked; industrialized countries must react promptly to plague outbreaks as well as other epidemic diseases, in order to inform the population and help fight against them. 10–16. It may have been an early appearance of smallpox that began with the Huns.The Huns then infected the Germans, who passed it to the Romans and then returning troops spread it throughout the Roman empire. After a small outbreak of plague in Taranto, Italy, in 1945, there was a large-scale anti-rodent campaign, which killed around 5000 rats . International Organization for Standardization (ISO) Country code in parentheses.). 336564 (PI Christos Lynteris, University of St Andrews). This was the third major bubonic plague outbreak to hit European society. The third, or modern, pandemic started in China in the 19th century and spread to many parts of the world in port cities. This bubonic plague pandemic started in the Yunnan province in China. A recent paper , which analysed plague cases reported since the end of the last century, has proposed classifying plague as a re-emerging disease. Verification of plague cases reported in October, 1907. More than 40% of adults in four states – Illinois, Louisiana, Mississippi and Missouri – and Washington, D.C., had symptoms of anxiety or depression. [21,63,72]). Despite the regulations in place, Europe experienced several outbreaks of plague during the Third Pandemic, but the vast majority of these outbreaks were small (electronic supplementary material, table S1). We describe important cases and outbreaks that took place during the Third Pandemic and the international efforts enacted to prevent the importation and spread of the disease. The two species are similar in appearance, but they have very different behaviour, as first described in a German zoological journal in 1952 by Eibl-Eibesfeldt  and later in great detail by Telle . Thucydides, in the History of the Peloponnesian War, paused in his narrative of the war to provide an extremely detailed description of the symptoms of those he observed to be afflicted; symptoms he shared as he too was struck by the illness. Bubonic plague symptoms and signs include painful and enlarged or swollen lymph nodes (an enlarged lymph node due to plague is called a bubo), chills, ... causing the death of 60% of the entire population. The digitization of international records of notifiable diseases, including plague, has enabled us to retrace the introductions of the disease to Europe from the earliest reported cases in 1899, to its disappearance in the 1940s. The earliest known European cases occurred in September and October 1896, when two sailors from Bombay died of plague on ships docked in London on the Thames . India was profoundly affected, resulting in 10 million deaths. Spanish flu that lasted from 1918 until 1920 was the deadliest pandemic ever. designed research; B.B. But it was another plague outbreak that would help shape China's future. Map of reported plague cases in Europe (1899–1947) from the Public Health Reports and electronic supplementary material, including the number of outbreaks in each location (see also the electronic supplementary material, table S1). Perhaps the most extensive rat surveys carried out during the Third Pandemic in Europe were in and around East Suffolk, Britain, where cases appeared regularly from 1906 to 1918 [36,44]. Casualties from the Third Plague Pandemic dropped to fewer than 200 per year in 1960. CC BY 4.0. Necrosis of the limbs was one of the terrifying symptoms. The conference was chaired by Dr Wu Lien Teh, who had stopped the great epidemic of pneumonic plague in Manchuria and Mongolia (about 60 000 victims) by 1910 . Indeed, during the nineteenth century, the spread of several diseases like tuberculosis, smallpox, cholera and yellow fever prompted extensive campaigns in European cities to improve hygienic conditions . ‘Liverpool Port Sanitary Authority rat-catchers dipping rats in buckets of petrol to kill fleas for plague control. Visuals Unlimited / Corbis. We declare we have no competing interests. Following the outbreak, the authorities trapped 148 rats, 14 were R. rattus and the rest were R. norvegicus, but they found no evidence of plague . Epidemic is a term that is often broadly used to describe any problem that has grown out of control. We are indebted to Giovangualberto Carducci, who has provided us with valuable published and unpublished material about the plague in Taranto 1945, and to the project Visual Representations of the Third Plague Pandemic, funded by a European Research Council Starting Grant under the European Union's Seventh Framework Programme/ERC grant agreement no. The second event was the discovery of two sailors from Bombay who died of plague on a ship in London in 1896 [21,32]. Of these, 60% were R. norvegicus and 40% were R. rattus in the docks, while all of the rats in the city were black rats. Yet, Europe still experienced plague outbreaks during the Third Pandemic, which began in China and spread globally at the end of the nineteenth century. For plague, detailed records of cases and deaths appear in the Public Health Reports beginning in 1899 (electronic supplementary material, table S1). The earliest cases popped up in the spring of 1665 and the death rate rose that summer. The European sanitary authorities responded by meeting often to discuss preventative measures against plague and other diseases. collected data and performed analyses; B.B. International conferences were held in Venice in 1892, in Dresden in 1893 and in Paris in 1894 . The third pandemic of plague (in its bubonic and pneumonic clinical forms) struck the globe between 1894 and 1959. Examination of rats for plague-infection, 1900–1907, The scarcity of rats and the Black Death: an ecological history, Rats cannot have been intermediate hosts for, Ethologische Unterschiede zwischen Hausratte und Wanderratte. Weeks later in Liverpool, a chain of deaths from plague began among the relatives and neighbours who handled the clothes worn by the two girls in Glasgow . second plague pandemic (14th–18th century). When plague was introduced to Europe during the Third Pandemic, rats were heavily scrutinized by European health authorities (figure 3) when plague cases were discovered (e.g. Published by the Royal Society under the terms of the Creative Commons Attribution License Reported suspected plague cases per year in Europe (1899–1950) from the Public Health Reports. These symptoms include fever, headaches, and vomiting. Our study area was continental Europe, excluding Russia, but including the Mediterranean islands. Finally, we would like to thank three anonymous referees whose comments have improved our contribution. The low number of human plague cases in Europe during the Third Pandemic could be explained by a low number of infected rats, but it could also be a reflection of effective public health intervention measures that reduced the contact between humans and infected vectors, such as isolation of patients and contacts, prohibition of gatherings and improved hygiene (e.g. The black rat has a history in Europe dating back to medieval times, but it has never been present in large numbers because the climate in Europe is too cold for it to be able to live and reproduce outside heated buildings . An epidemic is a broad term used to describe any problem that is actively spreading and has grown out of control. It reached the Byzantine capital of Constantinople in 541 A.D., and was soon claiming up to 10,000 lives per day—so many that unburied bodies were eventually stacked inside buildings or left in the open. The Third Plague Pandemic began in the 1850s in the Yunnan region of China. This is the new principle underlying modern international prophylaxis' [21, p. vi]. Despite the independency of these strains, the clinical symptoms were similar during the first and second pandemics. However, not all introductions of plague led to the formation of reservoirs, typically found in arid and semi-arid highlands , which are not present in Europe. The datasets supporting this article have been uploaded as part of the supplementary material (electronic supplementary material, table S1). The largest rat epizootic found in Marseille occurred in the poor downtown areas in 1930, where 42 infected rats were discovered out of the 7275 that were examined . Photograph, 1900/1920’. Although published in 1947 and a piece of fiction, The Plague by Albert Camus still eerily reflects how we reacted to the COVID-19 pandemic today as if it is a pattern that we need to recognize. Case records and outbreak reports for the Third Pandemic are numerous and have improved our understanding of the historical epidemiology and distribution of plague. Another key international plague conference was held in Shenyang (old name, Mukden) in April 1911, with epidemiologists and scientists from 11 countries (China, Japan, USA, Great Britain, France, Germany, Italy, Austria–Hungary, The Netherlands, Russia and Mexico) . These reports have been compiled and summarized for several regions: North America [22,23], South America [23,24], Africa [23,25] and Asia . However, some researchers have argued that the authorities were unlikely to find plague-infected rats because they would go into hiding , thus differing in their behaviour from the rats in Hong Kong during the outbreak of 1894, which were described as dead ‘in abundance on the streets and in the houses' [48, p. 311]. As it is still the case for today, vermin infestations back then were associated with poverty and unhygienic living conditions (e.g. 1–2]. The pattern of recurrent cases in East Suffolk led researchers John and Dorothy Black to assume that plague was endemic in this region . This necessitated the development of adequate measures to prevent the introduction and spread of infectious diseases to Europe. Plague was reported in 11 countries, and many cities, including Lisbon, Marseille, Paris and Pireas, experienced multiple outbreaks (table 1). Second plague pandemic and Third plague pandemic are connected through Timeline of plague, Pneumonic plague, Plague of Justinian and more.. Scheube wrote that, ‘The development and spread of plague is influenced in a great measure by the unfavorable hygienic conditions, essentially connected with social misery’ [75, p. 12]. Bubonic plague is one of three types of plague caused by the plague bacterium (Yersinia pestis). Map of reported plague cases in Europe (1899–1947) from the Public Health Reports and electronic supplementary material, including the number of outbreaks in each location (see also the electronic supplementary material, table S1).Download figureOpen in new tabDownload powerPoint. The authors acknowledge funding from the European Research Council under the European Union's Seventh Framework Programme/ERC grant agreement (AdG MedPlag, grant agreement no. 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