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KeywordsBubonic Plague Pandemic Yersinia pestis
The plague, otherwise notorious as the Black Death or the Pestilence, often regarded as a curse from God, has its place in every religious scripture. For Christians, it was divine punishment, for Muslims, a symbol of self-sacrifice (martyrdom). In the Hindu scripture (Bhagwat Purana), the plague was known as Mahamari, the “great death” which was caused by rats or rodents (Park 2000). Originated from a Greek word, plaga, meaning a blow or sudden strike, the Plague has a detailed description, including its clinical manifestations, in Thucydides’ The History of the Peloponnesian War (Crawley 2013; Rao 1994). It was recorded in the wake of the political struggle between Athens and Sparta. Plague broke out in its most lethal form, causing many deaths in Athens. It also caused total disruption of community ties and massive demoralization in society. Its impact on military and economic strength resulted in undermining civil and religious institutions at that time (Smith 1997).
The history of bubonic plague is documented among the Great Pandemics and is one of the historic diseases that killed over 200 million people in the world so far and continues to be synonymous with dread and fear. Plague had a devastating effect on the human civilizations starting from 542 B.C., when the disease affected the Nile valley and Egypt during the Pharaonic era. Archeozoological evidence suggests that the Nile rat was the original carrier of the disease (Panagiotakopulu 2004). Previously, it was advocated that the plague had a Central Asian origin.
Arguably, bubonic plague is one of the most feared and deadly infectious pestilence known to humankind until the late nineteenth century. There are three plague pandemics or major human outbreaks so far. The world witnessed the first plague pandemic in AD 541 during the reign of the Byzantine emperor Justinian I, and for almost six decades it caused widespread casualties (Rosen 2007; Retief and Cilliers 2005). The outbreak mostly affected the Mediterranean region and ravaged Constantinople (present-day Istanbul, Turkey). This pandemic witnessed the death of tens of millions of people and contributed to the fall of the Roman Empire. Its spread was chronicled by Byzantine historian Procopius. According to him, the epidemic entered Europe in 541 A.D. from the port of Pelusium (in Egypt).
The Second Pandemic in the fourteenth century devastated most of Europe and is estimated to have killed more than 25 million people. Notoriously and controversially termed as the Black Death, the disease lasted from 1347 and 1351, unfolding as the most violent epidemic in recorded history (Mackenzie 2001). It is widely believed that the spread of the disease to Europe was connected to one of the first recorded incidents of biological warfare, documented in the memoirs of the Italian Gabriele de’ Mussi. According to this work, soldiers of the Golden Horde (Mongols) catapulted corpses of plague victims into the besieged Genoese trading port of Caffa (now in Ukraine) on the Black Sea (Wheelis 2002; Derbes 1966). From here, the disease spread to Italy, Spain, England, France, and North Africa and soon engulfed Europe. Even after the great pandemic wore out, plague remained endemic among the rodent population, the primary vector of this deadly disease. As a result, the epidemic lingered on for centuries as the disease surfaced sporadically in Asia and Europe throughout the seventeenth century. The example of the Great Plague of London (1665–1666) was the deadliest reminder, an episode in which 70,000 people died.
The third pandemic was caused by the increasing human mobility with the movement of steamships. It started in the later part of the nineteenth century (1893–1894) in China and reached Indian shores in 1896, and subsequently other major port cities of the world. India had experienced plague before, in 1612, which primarily affected Agra city. It was in the modern or Third Pandemic era that India experienced the epidemic in its most virulent form, along with the United States and many South and Central Asian countries (Dhanukar and Hazra 1994). This pandemic reportedly killed more than 12 million people in China and India alone. In Egypt, it entered through the main ports, Alexandria and Port Said, around 1900. According to the World Health Organization, the third pandemic was considered active until 1959 as fatality rates diminished substantially to 200 per year. During this period, scientists identified and cultured the plague bacillus after thorough investigation and developed a crude vaccine.
Alexander Yersin first cultured the plague bacillus in Hong Kong in the mid-1890s, and it is now known as Yersinia pestis (formerly, Pasturella pestis) (Solomon 1995). A French scientist, while investigating the bubonic plague in Bombay, discovered the connection between rat, rat fleas (Xenopsylla cheopis), and the plague bacillus. Later, Waldemmar Haffkine developed an anti-plague vaccine, also in Bombay (now Mumbai in Maharashtra State, India). However, by this time, plague had spread around the globe except for Australia, and the endemic foci had established itself in rodent populations in almost every continent, irrespective of climatic conditions. Though the pandemic subsided gradually, it was the international regulations on rat control in ports and ships which mostly restricted the spread of plague disease. There were also several other preventive and control measures with the development of modern science and the use of disinfectants such as Dichloro-Diphenyl-Trichloroethane or DDT, adopted in later period of the third pandemic.
Bubonic Plague Etiology
What is plague? How are humans susceptible to it? The answers to these questions depict the etiology of plague. It is a zoonotic disease primarily spread to humans from its natural hosts, i.e., rats. The disease or infection cycle involves causative organisms (Yersinia pestis, hereafter Y.pestis), the reservoirs (Rats), the vector (fleas) and the human host. The most common carrier is the wild rat (Tatera indica). But the transmission occurs when there are some disturbances in the environment which facilitate contacts between wild rats and house rats (Rattus rattus) or the brown sewer rats (Rattus norvegicus) and field rats (Rattus argentiventer). It is also transmitted to rabbits and squirrels through rat fleas (Xenopsylla cheopis and X. brasiilensis). There are cases where unsuspecting huntsmen kill and eat these animals (such as infected or sick wildcats or marmots), thus becoming infected. This type of transmission is often termed as sylvatic plague.
There are three principal clinical manifestations of plague: bubonic, pneumonic, and septicemic. Bubonic plague is characterized by the swollen lymph nodes (buboes), mainly in the groin and less often in the neck and armpits, depending on the site of the flea bite. It cannot spread from person to person. Pneumonic plague involves the lungs and is highly infectious. It can spread among humans as the plague bacillus is present in the sputum of infected persons. The septicemic plague is very rare and only occurs when the bacilli invade the bloodstream (Park 2000). The disease starts with the rapid onset of fever and other systemic manifestations of gram-negative bacterial infection. Among these three-principal types of plague, pneumonic plague is more fatal, and patients who do not receive treatment within 18 h after the onset of symptoms are unlikely to survive. The patient goes through shock, multiple organ failure, and death.
Bubonic plague, which is of highest interest to this volume, reminds us about the Great Pestilence that wreaked havoc for centuries. It should be noted that the other manifestations, both septicemic and pneumonic forms, may be primary or secondary to bubonic disease. Irrespective of the mortality rates among these three types of plague infection, bubonic plague draws more fear and dread due to various reasons, including the physical manifestations of the disease on the human body.
Arguably the most common form, bubonic plague is typically caused by the bite of an infected flea (the vector) that has fed previously on a plague-infected animal, but it can also result from the consumption of infectious fluids. During an incubation period of 2–6 days, Y. pestis bacteria are transported from the initial bite site to the nearest lymph nodes that become swollen and tender, forming a bubo. Simultaneously, symptoms of blood poisoning or toxemia appear, including severe headache, chills, and fever accompanying physical fatigue. The final stage consists of shock and respiratory arrest, which occurs in 50–90% of untreated bubonic plague cases.
Naturally occurring plague is endemic in many regions of the world where the enzootic cycle involves numerous species of rodents and small mammals. According to one estimation, there are over 340 species of mammals that can be hosts to fleas, and nearly, 30 varieties of fleas can be transmitters of Y. pestis. When fleas feed on the infected animals, they suck out blood containing Y. pestis bacteria that then clog the upper gut of the flea. The flea attempts to bite other animals and humans subsequently regurgitating or discharging the bacteria-laden blood into the wound, infecting the victim.
Undoubtedly, the development in modern science and the pharmaceutical industry played a significant role in the successful management of the disease outbreak and the treatment of plague. For years, bubonic plague has been successfully treated with potent bactericidal antibiotics, such as streptomycin, gentamicin, doxycycline, and ciprofloxacin. However, a case of multiple antibiotic-resistant strains of Y. pestis occurred in Madagascar in 1995, and this brought attention to the issue of the long-term/future effectiveness of antibiotic treatment against the plague infection. At present, the antibiotic choices available can counter the emergence of resistant strains.
Although plague as a disease no longer causes alarm and is mostly wiped out from the major urban centers of the world, it still occurs around the world. The most endemic countries are, according to the WHO (World Health Organization), the Democratic Republic of the Congo, Madagascar (Africa), and Peru (South America). From 2010 to 2015, there were 3248 cases of plague reported worldwide, including 584 deaths (WHO 2017b).
The ensuing section of the article examines three brief case studies of bubonic plague outbreaks, with a view to their historical importance and other intriguing aspects: an urban epidemic (in London); the complexity of disease manifestations after years of quiescence (both of bubonic and pneumonic cases in Surat, India); and endemic challenges related to plague (such as in Madagascar).
The Great Plague of London
England was a plague-endemic country and it had a history of outbreaks of different intensity since the time of Black Death, or from 1348, up till 1665. Various descriptions of the disease symptoms and manifestations from 1665 and the recent DNA analysis of mass graves from the Bedlam burial ground dating to that period support the theory that Y. pestis was responsible for the 1665 epidemic. A significant proportion of samples tested positive for Y. pestis (Independent 2016, September 8).
The controversy around the origin of the outbreak notwithstanding, in the preceding years of the London Plague, a massive plague outbreak devastated cities in the Netherlands with nearly 35,000 deaths in Amsterdam alone. Researchers believe that the Dutch outbreak may have a connection with the London outbreak, either through human or animal connection. The bubonic plague that ravaged seventeenth century London (between 1665 and 1666) started from the city’s overcrowded northwestern outskirt St. Giles-in-the-Field. This was the worst plague outbreak since the Black Death of the fourteenth century. What started from St. Giles-in-the-Field, eventually engulfed the whole of London within 4 months and killed approximately 68,500 people as per available records. In total, the death toll reached somewhere between 75,000 and 100,000 by the end of this devastating pestilence (Porter 2009). The worst affected areas were located around the edge of the London city, besides St. Giles-in-the-Field, Cripplegate, Holborn, Bishopsgate, St. Botolph, and a few suburbs South of the Thames river, for example, Southwark (Porter 2009).
The great plague exposed London’s and, to that effect, England’s basic and struggling public health and inconsistent relief measures, mostly leaving the plague-affected people at the mercy of the prevalent “parish” and monastery system. The plague also disrupted the burgeoning trade and commerce in London which was already becoming a hub during that period.
Plague in Surat, India, 1994
The epidemic is not new to India or Indians. However, the reemergence of the disease in India in 1994 (in Surat, in Gujarat state) after several years of quiescence invoked a public health debate in the country. The plague which ravaged the Diamond City of Surat and scenic hamlets in Shimla affected the economic and political activity in the country, and also posed a serious question about the management of emerging and reemerging infectious diseases.
During the Third Plague Pandemic, India experienced the epidemic in 1895–1896, which continued for at least two decades, killing approximately ten million people. One estimate posits that it may have lasted up until 1950, with the number of deaths at 12.5 million (Ramalingaswami 1996). However, it is believed that after 1950, due to the emergence of many broad-spectrum antibiotics and disinfectants like DDT and Gamaxine, the spread/transmission of plague was contained. This period of quiescence (1967–1993) raised hopes that eradication may have been completed, and, along with that hope, complacency in the health administration. In the decade following this quiescence, India experienced plague outbreaks that took a heavy toll on India’s health infrastructure and urban management.
In India, empirical studies show that the plague occurs either in Spring or in Autumn, but at most times is interrupted by the hot Indian summer (Cohn 2002). The Surat plague outbreaks only confirmed this pattern. In Surat, the disease broke out in the month of September. It is believed that the earthquake in Beed district in 1993 disturbed the territorial equilibrium between wild rats and house rats, which facilitated fleas jumping their hosts. Also, a flood in the river Tapti during that time aggravated this nature-driven development (Parasuraman and Unnikrishnan 2000). Meanwhile, the growth in the city skyline and haphazard planning, increasing slums and unhygienic conditions, all combined to cause the epidemic. Surat came under the grip of the plague in both forms: bubonic and pneumonic. The official figure put the case-fatality rate at 752/44 by the end of September 1994 (CDC 1994a). Although Surat remained the epicenter of the plague outbreak, it spread to other parts of the country, primarily due to unrestricted human movement. In early September 1994, a bubonic plague outbreak occurred in Mamla village in Beed district of Maharashtra state. When the panic-stricken inhabitants fled the area, they carried the disease to other parts of India. Besides Surat, cases were reported from Maharashtra, Karnataka, Uttar Pradesh, Madhya Pradesh, and New Delhi (CDC 1994b). Further research confirmed the association of Y.pestis with the epidemic in Surat and Beed, and demonstrated that Y.pestis had an enzootic existence in the region (Panda 1996).
Plague in Madagascar (1995–2017)
Bubonic plague remains a significant public health challenge in Madagascar It is endemic in Madagascar, especially to the central and northern highlands. The disease found its way to Madagascar in 1898 via the port of Toamasina, reaching the island by steamboats from India, and by 1921 it reached the capital Antananarivo. The disease mostly remained under control between 1928 and 1990.
However, a first major outbreak occurred in 1991 around the coastal town of Mahajanga. From 1995 to 1998, outbreaks of bubonic plague occurred annually in the coastal city of Mahajanga. A total of 1,702 clinically suspected cases of bubonic plague were reported, including 515 laboratory-confirmed cases of Y. pestis infection. The epicenters of the outbreaks were usually crowded and unhygienic districts with proximity among human and rodent populations.
Available records show that from 1998 to 2016, a total of 13,234 suspected cases were recorded, mainly from the central highlands; 27% were confirmed cases, and 17% were presumptive cases. Patients with bubonic plague represented 93% of confirmed and presumptive cases, and patients with pneumonic plague represented 7% (Andrianaivoarimanana et al. 2019). Besides Mahajanga, Mandritsara city was worst affected in 2013, when the bubonic plague killed 39 villagers despite an early warning in October from the International Committee of the Red Cross (ICRC) about the impending risk of a plague epidemic (The National 2013). The last major plague outbreak occurred in the beginning of August, 2017, primarily affecting the capital Antananarivo and the central port city of Toamasina. The outbreak lasted until November 22, 2017, with a total of 2348 confirmed, probable and suspected cases of plague (1791 cases of pneumonic, 341 cases of bubonic and one case of septicemic plague). There were also 215 unspecified cases. Over 200 people died of the infections (WHO 2017a). This rise in pneumonic plague cases caused concern with a view to the possible future reemergence and rapid spread of plague in urban settings.
In the words of Ira Klein, “Plague was a savage cause of death and, equally, of social turmoil and conflict between State and populace” (Klein 1988). Though rightly observed, bubonic plague outbreaks taught valuable lessons to the ever-complacent humankind in the sphere of public health with regards to disease surveillance and epidemic management, teaching us lessons that we had better keep in mind even in the present day.
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