Page 11Volume 20 Number 2; April 2012
Pastorien and a French naval doctor, demonstrated
that the Oriental rat flea was the vector for the
bacillus and the sources of the bacillus were the
sewer rats.3,4
The germ, the rats, and the fleas
Yersinia pestis is most likely a clone that evolved
some 1,500 to 20,000 years ago from a common
ancestor with Yersinia pseudotuberculosis, an animal
enteropathogen which does not cause blood infection
or plague. The bacillus probably arose in Asia,
although it had been present in east-central Africa for
the past two millennia and probably longer.2, 5
There
are three biovars of the bacillus based on phenotypic
differences, Antiqua, Medievalis, and Orientalis, and
it has been postulated that they were responsible for
the first, second and third pandemics respectively.
A paleomicrobiological analysis by Drancourt et al
in 2004 however indicated that all three pandemics
were most likely caused by the Orientalis biovar.6, 7
There had also been debate for some time whether the
Justinian and the Black Death plagues were actually
due to Yersinia pestis and were not instead epidemic
haemorrhagic fevers3,8
. Analyses by Drancourt and
others have found evidence of the plague bacillus
in specimens of persons known to have died in
the first two pandemics. It is also very difficult to
discount the vivid and accurate descriptions of the
bubonic plague that were given by historians such
as Procopius of Caesarea, Gabriel de Mussis and
Giovanni Boccaccio.
The vector host in the Black Death pandemic was
Rattus rattus - the ‘old English’ or black rat. The
black rat originated in India and migrated along
the Silk Road from Asia to the Middle East, and
then travelled in ships on the sea trade routes,
settling in most areas of the world and cohabitating
comfortably with humans in their houses, factories,
and dockyards. The black rat had probably acquired
the disease from contact with infected wild rodents
from the steppes of Central Asia and Russia, and
in fact the disease may have been transported in
infested marmot hides taken by Tartar hunters
from Manchuria. The brown or sewer rat, Rattus
norvegicus, didn’t become prevalent in the Western
world until the 18th century. It originated in Central
The History of Plague – Part 1.
The Three Great Pandemics
John Frith
Plague is an acute infectious disease caused by
the bacillus Yersinia pestis and is still endemic in
indigenous rodent populations of South and North
America, Africa and Central Asia. In epidemics
plague is transmitted to humans by the bite of the
Oriental or Indian rat flea and the human flea. The
primary hosts of the fleas are the black urban rat and
the brown sewer rat. Plague is also transmissible
person to person when in its pneumonic form.
Yersinia pestis is a very pathogenic organism to both
humans and animals and before antibiotics had a
very high mortality rate. Bubonic plague also has
military significance and is listed by the Centers
for Disease Control and Prevention as a Category A
bioterrorism agent.1
There have been three great world pandemics of
plague recorded, in 541, 1347, and 1894 CE, each
time causing devastating mortality of people and
animals across nations and continents. On more
than one occasion plague irrevocably changed the
social and economic fabric of society.
In most human plague epidemics, infection initially
took the form of large purulent abscesses of lymph
nodes, the bubo (L. bubo = ‘groin’, Gr. boubon =
‘swelling in the groin’), this was bubonic plague. When
bacteraemia followed, it caused haemorrhaging and
necrosis of the skin rapidly followed by septicaemic
shock and death, septicaemic plague. If the disease
spread to the lung through the blood, it caused an
invariably fatal pneumonia, pneumonic plague, and
in that form plague was directly transmissible from
person to person.
The three great plague pandemics had different
geographic origins and paths of spread. The Justinian
Plague of 541 started in central Africa and spread to
Egypt and the Mediterranean. The Black Death of
1347 originated in Asia and spread to the Crimea
then Europe and Russia. The third pandemic, that
of 1894, originated in Yunnan, China, and spread to
Hong Kong and India, then to the rest of the world.2
The causative organism, Yersinia pestis, was not
discovered until the 1894 pandemic and was
discovered in Hong Kong by a French Pastorien
bacteriologist, Alexandre Yersin. Four years later
in 1898 his successor, Paul-Louis Simond, a fellow
History
Page 12 Journal of Military and Veterans’ Health
Asia and migrated westward on the sea routes from
China and India. The brown rat flourished in Europe
where there were open sewers and ample breeding
grounds and food and in the 18th and 19th centuries
replaced the black rat as the main disease host.4, 9
The primary vectors for transmission of the disease
from rats to humans were the Oriental or Indian
rat flea, Xenopsylla cheopis, and the Northern
or European rat flea, Nosopsyllus fasciatus. The
human flea, Pulex irritans, and the dog and cat fleas,
Ctenocephalides canis and felis, were secondary
vectors. In the pandemics, the infected fleas were
able to spread the plague over long distances as
they were carried by rats and by humans travelling
along trade routes at sea and overland, and also by
infesting rice and wheat grain, clothing, and trade
merchandise. When infected, the proventriculus
of the flea becomes blocked by a mass of bacteria.
The flea continues to feed, biting with increasing
frequency and agitation, and in an attempt to relieve
the obstruction the flea regurgitates the accumulated
blood together with a mass of Yersinia pestis bacilli
directly into the bloodstream of the host. The fleas
multiply prolifically on their host and when the host
dies they leave immediately, infesting new hosts and
thus creating the foundations for an epidemic.10, 11
The Justinian Plague of 541-544
The first great pandemic of bubonic plague
where people were recorded as suffering from the
characteristic buboes and septicaemia was the
Justinian Plague of 541 CE, named after Justinian
I, the Roman emperor of the Byzantine Empire at
the time. The epidemic originated in Ethiopia in
Africa and spread to Pelusium in Egypt in 540. It
then spread west to Alexandria and east to Gaza,
Jerusalem and Antioch, then was carried on ships
on the sea trading routes to both sides of the
Mediterranean, arriving in Constantinople (now
Istanbul) in the autumn of 541.12, 13
The Byzantine court historian, Procopius of
Caesarea, in his work History of the Wars, described
people with fever, delirium and buboes He wrote that
the epidemic was one ‘by which the whole human
race came near to be annihilated’. Procopius wrote
of the symptoms of the disease :
“ ... with the majority it came about
that they were seized by the disease
without becoming aware of what was
coming either through a waking vision
or a dream. ... They had a sudden fever,
some when just roused from sleep,
others while walking about, and others
while otherwise engaged, without any
regard to what they were doing. And
the body showed no change from its
previous colour, nor was it hot as
might be expected when attacked by a
fever, nor indeed did any inflammation
set in, but the fever was of such a
languid sort from its commencement
and up till evening that neither to the
sick themselves nor to a physician
who touched them would it afford any
suspicion of danger. It was natural,
therefore, that not one of those who had
contracted the disease expected to die
from it. But on the same day in some
cases, in others on the following day,
and in the rest not many days later, a
bubonic swelling developed; and this
took place not only in the particular
part of the body which is called boubon,
that is, “below the abdomen,” but also
inside the armpit, and in some cases
also beside the ears, and at different
points on the thighs.”14
The focus of the Justinian pandemic was
Constantinople, reaching a peak in the spring of 542
with 5,000 deaths per day in the city, although some
estimates vary to 10,000 per day, and it went on
to kill over a third of the city’s population. Victims
were too numerous to be buried and were stacked
high in the city’s churches and city wall towers,
their Christian doctrine preventing their disposal by
cremation. Over the next three years plague raged
through Italy, southern France, the Rhine valley and
Iberia. The disease spread as far north as Denmark
and west to Ireland, then further to Africa, the
Middle East and Asia Minor. Between the years 542
and 546 epidemics in Asia, Africa and Europe killed
nearly 100 million people.15, 16
The pandemic had a drastic effect and permanently
changed the social fabric of the Western world. It
contributed to the demise of Justinian’s reign. Food
production was severely disrupted and an eight year
famine followed. The agrarian system of the empire
was restructured to eventually become the three field
feudal system. The social and economic disruption
caused by the pandemic marked the end of Roman
rule and led to the birth of culturally distinctive
societal groups that later formed the nations of
medieval Europe.12
Further major outbreaks occurred throughout
Europe and the Middle East over the next 200
years - in Constantinople in the years 573, 600, 698
and 747, in Iraq, Egypt and Syria in the years 669,
683, 698, 713, 732 and 750 and Mesopotamia in
686 and 704. In 664 plague laid waste to Ireland,
History
Page 13Volume 20 Number 2; April 2012
and in England it came to be known as the Plague
of Cadwaladyr’s Time, after a Welsh king who
contracted plague but survived it in 682. The plague
continued in intermittent cycles in Europe into the
mid-8th century and did not re-emerge as a major
epidemic until the 14th century.
The ‘Black Death’ of Europe in 1347 to 1352
The Black Death of 1347 was the first major European
outbreak of the second great plague pandemic that
occurred over the 14th to 18th centuries. In 1346 it
was known in the European seaports that a plague
epidemic was present in the East. In 1347 the plague
was brought to the Crimea from Asia Minor by the
Tartar armies of Khan Janibeg, who had laid siege
to the town of Kaffa (now Feodosya in Ukraine), a
Genoese trading town on the shores of the Black Sea.
The siege of the Tartars was unsuccessful and before
they left, from a description by Gabriel de Mussis
from Piacenza, in revenge they catapulted over the
walls of Kaffa corpses of people who had died from
the Black Death. In panic the Genoese traders fled
in galleys with ‘sickness clinging to their bones’ to
Constantinople and across the Mediterranean to
Messina, Sicily, where the great pandemic of Europe
started. By 1348 it had reached Marseille, Paris and
Germany, then Spain, England and Norway in 1349,
and eastern Europe in 1350. The Tartars left Kaffa
and carried the plague away with them spreading it
further to Russia and India.17
A description of symptoms of the plague was given by
Giovanni Boccaccio in 1348 in his book Decameron,
a set of tales of a group of Florentines who secluded
themselves in the country to escape the plague :
“.. in men and women alike it first
betrayed itself by the emergence of
certain tumours in the groin or armpits.
Some of which grew as large as a
common apple, others as an egg, some
more, some less, which the common folk
called gavocciolo. From the two said
parts of the body this deadly gavocciolo
soon began to propagate and spread
itself in all directions indifferently; after
which the form of the malady began
to change, black spots or livid making
their appearance in many cases on the
arm or the thigh or elsewhere,..“17
The term “Black Death” was not used until much
later in history and in 1347 was simply known as
“the pestilence” or “pestilentia”, and there are various
explanations of the origin of the term. Butler [11]
states the term refers to the haemorrhagic purpura
and ischaemic gangrene of the limbs that sometimes
ensued from the septicaemia. Ziegler17
states it
derives from the translation of the Latin pestis atra
or atra mors, ‘atra’ meaning ‘terrible’ or ‘dreadful’,
the connotation of which was ‘black’, and ‘mors’
meaning ‘death’, and so ‘atra mors’ was translated
as meaning ‘black death’.
The social impacts of the Black Death in Europe
during the 14th century
The overall mortality rate varied from city to city, but
in places such as Florence as observed by Boccaccio
up to half the population died, the Italians calling the
epidemic the mortalega grande, ‘the great mortality’.
[18]
People died with such rapidity that proper burial
or cremation could not occur, corpses were thrown
into large pits and putrefying bodies lay in their
homes and in the streets. People were as much
afraid they would suffer a spiritual death as they
were a physical death since there were no clergy to
perform burial rites:
“Shrift there was none; churches and
chapels were open, but neither priest
nor penitents entered – all went to
the charnelhouse. The sexton and
the physician were cast into the same
deep and wide grave; the testator and
his heirs and executors were hurled
from the same cart into the same hole
together.”18
Transmission of the disease was thought to be by
miasmas, disease carrying vapours emanating from
corpses and putrescent matter or from the breath of
an infected or sick person. Others thought the Black
Death was punishment from God for their sins and
immoral behaviour, or was due to astrological and
natural phenomena such as earthquakes, comets,
and conjunctions of the planets. People turned to
patron saints such as St Roch and St Sebastian or to
the Virgin Mary, or joined processions of flagellants
whipping themselves with nail embedded scourges
and incanting hymns and prayers as they passed
from town to town.17, 19, 20
“When the flagellants – they were
also called cross brethren and cross
bearers – entered a town, a borough or
a village in a procession their entry was
accompanied by the pealing of bells,
singing, and a huge crowd of people. As
they always marched two abreast, the
procession of the numerous penitents
reached farther than the eye could see.”
[20]
The only remedies were inhalation of aromatic
vapours from flowers and herbs such as rose,
History
Page 14 Journal of Military and Veterans’ Health
theriaca, aloe, thyme and camphor. Soon there was
a shortage of doctors which led to a proliferation of
quacks selling useless cures and amulets and other
adornments that claimed to offer magical protection.
In this second pandemic, plague again caused great
social and economic upheaval. Often whole families
were wiped out and villages abandoned. Crops
could not be harvested, travelling and trade became
curtailed, and food and manufactured goods became
short. As there was a shortage of labour, surviving
villager labourers, the ‘villeins’, extorted exorbitant
wages from the remaining aristocratic landowners.
The villeins prospered and acquired land and
property. The plague broke down the normal divisions
between the upper and lower classes and led to the
emergence of a new middle class.17, 9
The plague
lead to a preoccupation with death as evident from
macabre artworks such as the ‘Triumph of Death’ by
Pieter Breughel the Elder in 1562, which depicted in
a panoramic landscape armies of skeletons killing
people of all social orders from peasants to kings and
cardinals in a variety of macabre and cruel ways.
In the period 1347 to 1350 the Black Death killed a
quarter of the population in Europe, over 25 million
people, and another 25 million in Asia and Africa.[15]
Mortality was even higher in cities such as Florence,
Venice and Paris where more than half succumbed
to the plague. A second major epidemic occurred
in 1361, the pestis secunda, in which 10 to 20% of
Europe’s population died.13
Other virulent infectious
disease epidemics with high mortalities occurred
during this time such as smallpox, infantile diarrhoea
and dysentery. By 1430, Europe’s population was
lower than it had been in 1290 and would not recover
the pre-pandemic level until the 16th century.13, 21
Quarantine
In 1374 when another epidemic of the Black Death
re-emerged in Europe, Venice instituted various
public health controls such as isolating victims from
healthy people and preventing ships with disease
from landing at port. In 1377 the republic of Ragusa
on the Adriatic Sea (now Dubrovnik in Yugoslavia)
established a ships’ landing station far from the city
and harbour in which travellers suspected to have
the plague had to spend thirty days, the trentena, to
see whether they became ill and died or whether they
remained healthy and could leave. The trentena was
found to be too short and in 1403 in Venice, travellers
from the Levant in the eastern Mediterranean were
isolated in a hospital for forty days, the quarantena
or quaranta giorni, from which we derive the term
quarantine.8,18
This change to forty days may have
also been related to other biblical and historical
references such as the Christian observance of Lent,
the period for which Christ fasted in the desert, or
the ancient Greek doctrine of “critical days” which
held that contagious disease will develop within 40
days after exposure.22
In the 14th and 15th centuries
following, most countries in Europe had established
quarantine, and in the 18th century Habsburg
established a cordon sanitaire, a line between
infected and clean parts of the continent which ran
from the Danube to the Balkans. It was manned
by local peasants with checkpoints and quarantine
stations to prevent infected people from crossing
from eastern to western Europe.8
The leather costume of the plague doctors at
Nijmegen
In the 15th and 16th centuries doctors wore a
peculiar costume to protect themselves from the
plague when they attended infected patients, first
illustrated in a drawing by Paulus Furst in 1656
and later Jean-Jacques described a similar costume
worn by the plague doctors at Nijmegen, an old
Dutch town in Gelderland, in his 1721 work Treatise
on the Plague. They wore a protective garb head to
foot with leather or oil cloth robes, leggings, gloves
and hood, a wide brimmed hat which denoted their
medical profession, and a beak like mask with glass
eyes and two breathing nostrils which was filled with
aromatic herbs and flowers to ward off the miasmas.
They avoided contact with patients by taking their
pulse with a stick or issued prescriptions for aromatic
herb inhalations passing them through the door, and
buboes were lanced with knives several feet long.19
The Great Plague of London of 1665 to 1666
Plague continued to occur in small epidemics
throughout the world but a major outbreak of the
pneumonic plague occurred in Europe and England
in 1665 to 1666. The epidemic was described by
Samuel Pepys in his diaries in 1665 and by Daniel
Defoe in 1722 in his A Journal of a Plague Year.
People were incarcerated in their homes, doors
painted with a cross. The epidemic reached a peak
in September 1665 when 7,000 people per week were
dying in London alone. Between 1665 and 1666 a
fifth of London’s population died, some 100,000
people.[17]
The Great Fire of London in 1666 and the
subsequent rebuilding of timber and thatch houses
with brick and tile disturbed the rats’ normal habitat
and led to a reduction in their numbers, and may
have been a contributing factor to the end of the
epidemic.9
An old English nursery rhyme published in Kate
Greenaway’s book Mother Goose 1881 reminds us of
the symptoms of the plague :
History
Page 15Volume 20 Number 2; April 2012
‘Ring, a-ring, o’rosies, (a red blistery rash)
A pocket full of posies (fragrant herbs
and flowers to ward off the ‘miasmas’)
Atishoo, atishoo (the sneeze and the
cough heralding pneumonia)
We all fall down.’ (all dead)
Plague waxed and waned in Europe until the late 18th
century, but not with the virulence and mortality of
the 14th century European Black Death.
The Third Pandemic of 1894
The plague re-emerged from its wild rodent reservoir
in the remote Chinese province of Yunnan in 1855.
From there the disease advanced along the tin and
opium routes and reached the provincial capital of
K’unming in 1866, the Gulf of Tonkin in 1867, and
the Kwangtung province port of Pakhoi (now Peihai)
in 1882. In 1894 it had reached Canton and
then spread to Hong Kong. It had spread to Bombay
by 1896 and by 1900 had reached ports on every
continent, carried by infected rats travelling the
international trade routes on the new steamships.3,23
It was in Hong Kong in 1894 that Alexandre Yersin
discovered the bacillus now known as Yersinia pestis,
and in Karachi in 1898 that Paul-Louis Simond
discovered the brown rat was the primary host and
the rat flea the vector of the disease.3, 4, 24, 25
In 1900 the plague came to Australia where the first
major outbreak occurred in Sydney, its epicentre at
the Darling Harbour wharves, spreading to the city,
Surry Hills, Glebe, Leichhardt, Redfern, and The
Rocks, and causing 100 deaths. John AshburtonThompson,
the chief medical officer, recorded the
epidemic and confirmed that rats were the source
and their fleas were the vectors in the epidemic.
There were 12 major outbreaks of plague in Australia
from 1900 to 1925 with 1371 cases and 535 deaths,
most cases occurring in Sydney.26
The third pandemic waxed and waned throughout
the world for the next five decades and did not end
until 1959, in that time plague had caused over 15
million deaths, the majority of which were in India.
There have been outbreaks of plague since, such as
in China and Tanzania in 1983, Zaire in 1992, and
India, Mozambique and Zimbabwe in 199415, 27.
In
Madagascar in the mid-1990’s, a multi-drug resistant
strain of the bacillus was identified15, 28.
Currently
around 2,000 cases occur annually, mostly in Africa,
Asia and South America, with a global case fatality
rate of 5% to 15%.28
Bubonic plague is a virulent disease with a significant
mortality rate, transmitted primarily by the bite of
the rat flea or through person-to-person when in
its pneumonic form. There have been innumerable
epidemics of plague throughout history, but it was
the pandemics of the 6th, 14th and 20th centuries
that have had the most impact on human society,
not only in terms of the great mortalities, but also
the social, economic and cultural consequences that
resulted. The course of development of communities
and nations was altered several times. Much has
changed to prevent the recurrence of pandemic
plague, such as the development of the germ theory
and the science of bacteriology, public health
measures such as quarantine, and antibiotics
such as streptomycin, but plague today is still an
important and potentially serious threat to the
health of people and animals.
Author’s Affiliation: Australian Defence Force
Contact author: John Frith
Email: jfrith@unwired.com.au
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History