The Third Plague Pandemic in Europe

(a). Role of rats and other sources of plague

At the beginning of the Third Pandemic, physicians and scientists used new methods to increase their knowledge of plague, including microbiological and experimental techniques [45]. From the late 1800s, Lowry [46], Rocher [47] and Yersin [48], among others, observed a connection between human and rat plague mortality during epidemics in India and China, suggesting that black rats were involved in transmission. This observation was later confirmed by Simond, who demonstrated in 1897 that rat-fleas were vectors for the disease [49,50]. The prevailing view among researchers in the Indo-Pacific region, including Thompson [51] who observed plague outbreaks in Sydney, Hunter who reported on plague in Hong Kong [52] and those of the Indian Plague Commission [53], 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 [54]. 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. [36,37,55], see also the electronic supplementary material).

There were two species of commensal rats present in Europe during the Third Pandemic, the black rat (Rattus rattus), also called the ship rat or the roof rat, and the brown rat (Rattus norvegicus), also called the sewage rat. 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 [56]. The brown rat came to Europe from Russia during the early part of the eighteenth century and was abundant in all European cities around 1900 [57,58]. 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 [59] and later in great detail by Telle [60]. The American zoologist Davis [56] described similar differences in articles from the mid-1950s. The British zoologist Twigg later describes these differences in his book on ‘The Black Death’ [61]. These sources state that the black rat is an efficient climber, which makes nests in the walls and roofs of buildings, while the brown rat may live outdoors in the European climate, is an efficient swimmer, and makes nests in borrows in the soil, in cellars or in sewage pipes [57,59]. The two species of rats carry the same species of fleas. Owing to their different behaviour, black rats are living closer to humans than brown rats. During the Third Pandemic, plague was transported around the world by black rats on ships. At this time, black rats were not generally found in Europe, except in warehouses in ports and in a few towns [62].

From the first reports of plague, European sanitary authorities actively searched for dead rats in cities [39,63–66], urban districts [36,44], isles [67–70] and on ships [19], and they used early bacteriological methods to test for the plague bacterium in the local black and brown rat populations (e.g. [36,39,43,63–68,70]). For instance, when plague broke out in Glasgow in 1900 (see the electronic supplementary material), the Medical Officer of Health caught and examined 326 rats, but found no evidence of plague in the rat population [39,63]. They wrote after the outbreak that ‘inquiry failed to discover any evidence that rat mortality prevailed to an unusual extent’ [63, p. 26]. However, in the years following the outbreak, they found some evidence of plague in the rat population: in 1901 (122 of 1641), in 1902 (30 of 6492) and in 1907 (1 of 140) [55].

Rats were also examined during and after outbreaks in East Suffolk [36,44], Malta [67–69], Italy [66], Corsica [70], Spain [65] and France [64] (see the electronic supplementary material). After a small outbreak of plague in Taranto, Italy, in 1945, there was a large-scale anti-rodent campaign, which killed around 5000 rats [42]. 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. In 1945, they found only two rats tested positive [66] and, in 1946, none were infected [43]. There was a similar outbreak in Ajaccio, Corsica, on 12 May 1945, with 13 cases of plague reported over 10 weeks [71]. It was rumoured that dead rats were observed before the outbreak, but none were examined. 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 [70]. Rat monitoring was also carried out in Marseille, France, where 132 cases of plague were reported from 1919 to 1929 [64]. 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 [64].

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]. The pattern of recurrent cases in East Suffolk led researchers John and Dorothy Black to assume that plague was endemic in this region [36]. Surveys for plague were carried out over an area of more than 2000 km² [36,44]. However, only 60 plague-infected rats were found out of more than 266 000 rats that were caught during the 3 year survey [36,44]. In addition to rats, the authorities found some ferrets, cats and rabbits that died of plague [44]. 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].

Other documented sources of plague in Europe were from direct human transmission of pneumonic plague (e.g. [36,44,63]) and the transportation of infected vectors (e.g. [36,63]) (electronic supplementary material, table S1). Pneumonic plague occurs when plague infects the lungs, either primarily by the spread of infectious droplets or secondarily as a complication of bubonic plague. Cases of pneumonic plague were reported during many of the outbreaks in Europe (electronic supplementary material, table S1) and often spread within households and among close contacts [36,44]. For example, in East Suffolk, a 9-year-old girl became ill with pneumonic plague and died in a cottage 5 miles from Ipswich on 13 September 1910 [36,44]. Her mother also contracted the disease and died 3 days after her daughter's death, followed by her stepfather and a neighbour who nursed her mother. To prevent further spread, the funeral services of the victims were held in open air and the contacts of the deceased were isolated [36,44].

There are also accounts of bubonic plague transmission without a clear association with rats, probably from infected vectors (e.g. [39,63,72]). Many different flea species can carry and transmit plague, such as those commonly found on rats (Xenopsylla cheopis), cats (Ctenocephalides felis) and humans (Pulex irritans) [21]. Ectoparasites were so abundant in Europe that the Third International Congress on School Hygiene held in Paris in 1910 advised to fight against them, because one out of every three children was infested [73]. As it is still the case for today, vermin infestations back then were associated with poverty and unhygienic living conditions (e.g. [36,63,64,67,74]), often in the poorest quarters of cities, where the majority of cases were found during outbreaks such as Oporto (1899), Glasgow (1900) and Marseille (1900–1921). 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]. In some cases, it appears that infected vectors transmitted the disease between people in close contact. For example, during the plague in Glasgow in 1901, a woman who had fallen ill with the plague was visited by two friends from Liverpool [38] (see the electronic supplementary material). 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 [38]. Indeed, infected ectoparasites in clothing, rags, grain sacks and other textiles could explain the appearances of plague even in the absence of infected rats (e.g. [21,38,63]).

Overall, the connection between urban rodents and human plague in Europe during the Third Pandemic is less clear than for outbreaks in India and China [21,46,48–50,54,75–78]. However, it was often proposed that other sources of plague, such as infected human-specific or human-biting parasites, like fleas and lice, were important for transmission in Europe during the Third Pandemic [21,36,63,64,74]. The low numbers of plague-infected rats found during European outbreaks suggest that they played a relatively minor role in plague transmission. However, some researchers have argued that the authorities were unlikely to find plague-infected rats because they would go into hiding [51], 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]. 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. [21,63,72]).

(b). Disappearance of plague

Plague is not a disease that is found in Europe today, and we found no mention of plague outbreaks after 1950. The disappearance of plague in Europe during the Third Pandemic can be attributed to two main factors, improved hygiene and the lack of a present-day sylvatic reservoir for the disease.

At the end of the nineteenth century, the newly established discipline of microbiology found causative relationships between germs and diseases. In 1897, Proust observed that, ‘It is no matter of doubt that the plague cannot produce nowadays the disasters of the Black Death in the 14th c. Fortunately, the general hygienic conditions have much changed’ [21, pp. 1–2]. 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 [79]. In many places in Europe, this work included the destruction of slums, improvement of sewage systems and the widespread development of safe water supply systems [79].

Contemporary scholars regarded cleaning and disinfecting as an essential part of plague control measurements [21,67,80]. Proust described in Bombay that in places where it was possible to clean dwellings, houses and streets, plague outbreaks could be contained or avoided [21]. Indeed, from the 1950s, the introduction of baths in the majority of European dwellings, and the use of vacuum cleaners and washing machines, strongly enhanced personal hygiene and that of the domestic environment (e.g. [81]). 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 [69]. In Taranto in 1945, the allied forces, contributed noticeably to the fight against the epidemic by spraying large quantities of DDT against ‘fleas, but also bugs, lice and ticks' [66, p. 167].

Although the existence of a rodent reservoir for plague in the past is heavily debated [8,14,17,56,82–84], there is no evidence that plague is endemic to Europe today or was at any time during the Third Pandemic. Introductions of plague during the Third Pandemic led to the formation of plague reservoirs in the USA [22,23], South America (Peru, Bolivia and Brazil) [23,24] and Africa (Democratic Republic of the Congo, Tanzania, Uganda and Madagascar) [23,25], where ecological conditions have favoured the persistence of the bacteria in sylvatic rodent communities. Today, the spillover of plague from these reservoirs leads to the thousands of cases of plague reported every decade [85]. However, not all introductions of plague led to the formation of reservoirs, typically found in arid and semi-arid highlands [17], which are not present in Europe. The lack of a rodent reservoir in Europe is the fundamental reason why plague is no longer a public health threat today on the continent. The unfavourable environmental conditions in western Europe make it very unlikely that there has been a wild plague reservoir there. Even in Malta, where the environment is much more favourable to rodent reproduction [67], Barnett observed that ‘plague outbreaks always come to an end even if nothing is done to kill rats or their fleas’ [67, p. 17]. It is possible that future ancient DNA studies will demonstrate that all of the different lineages of Y. pestis involved in historic outbreaks went extinct after their introduction into Europe (see also Namouchi et al. [4]).