Did Yersinia pestis really cause Black Plague? Part 4: Plague in modern times

Though there still may be some lingering doubt about the cause of the Black Death and subsequent outbreaks of plague, the pathogen behind the outbreaks that have taken place in the last 150 years or so is much less ambiguous.

While Koch and Pasteur ushered in the golden age of microbiology, an outbreak of plague began in China and spread from there. In 1894, while plague was raging in Hong Kong, the Pasteur Institute sent Alexandre Yersin, a physician who had trained with both Pasteur and Koch, to investigate. Yersin was able to access material from a corpse, and inoculated material he withdrew from a deceased soldier's bubo into guinea pigs. His examination of the material revealed bacteria that were gram-negative: that is, they ended up pink when the Gram stain was carried out.

The guinea pigs Yersin inoculated died, and upon necropsy, he saw the same gram negative bacteria he'd found in the deceased soldier. He also was intrigued by the large numbers of dead rats he saw in the city (and even in the hospital). Upon examination, he saw the rats also were infected with these bacteria--concluding that the bacterium could infect both humans and other animal species.

However, Yersin didn't finish figuring out the transmission of the bacterium. Another researcher, Paul-Louis Simond, experimented using infected rats and fleas, and noted that even if a sick rat was placed in a jar with healthy rats, the healthy rats didn't typically become sick in the absence of fleas--suggesting fleas could act as an intermediate between infected and healthy animals, or between sick animals and the human population.

Remnants of this outbreak of plague, beginning in the mid-1860s, are still with us, as the bacterium rapidly spread across the globe by train and boat. And though most human cases are of the bubonic type, a handful of outbreaks of pneumonic plague have been documented in the last century. For example, in 1910-11, and again a decade later, two large outbreaks of pneumonic plague hit in Manchuria and China, erupting and spreading rapidly in the crowded conditions. Approximately 60,000 deaths were estimated from the first outbreak alone.

More recently, a 1994 outbreak of pneumonic plague in India resulted in over 600 confirmed cases and over 50 deaths. However, even worse than the death toll was the panic plague brought to the country, which had been plague-free since 1966. Physicians fled the area, and the outbreak severely affected the economy. I've seen estimates of the cost to tourism and trade range from $600 million up to $4 billion, so even with a relatively small outbreak, it has the potential to be a serious matter for the health of both the population and the economy.

Blogging on Peer-Reviewed Research Plague is considered a re-emerging disease. This means that it's not only still with us, but it's increasing in many geographic areas (particularly in Africa, including 2005 and 2006 outbreaks of pneumonic plague in the Democratic Republic of Congo [DRC]). And the U.S. isn't exempt. This review, for example, details outbreaks in 1919 and 1924 in Los Angeles. And while human plague is infrequent enough to make news when it pops up in the United States (we average ~10-20 cases per year, mostly in the southwest where plague is endemic in animals), it can still be fatal if not treated quickly. Worldwide, between 1000 and 5000 cases of plague are reported every year, with 100-200 deaths (and these likely represent only a fraction of the actual cases each year). Though the epicenter of plague cases used to be Asia, in the past 20 years most cases have occurred in Africa, especially the DRC, Uganda, and Madagascar, which has experienced a recent outbreak of plague.

There are concerns that we may see more plague in the future as well. A new review in PLoS Medicine suggests that global warming could seed additional plague pandemics:

Recent analysis of data from Kazakhstan shows that warmer springs and wetter summers increase the prevalence of plague in its main host, the great gerbil. Such environmental conditions also seem to have prevailed during the emergence of the Second and Third Pandemics--conditions that might become more common in the future.

This could happen in the U.S. also, since the same warm, wet conditions that can lead to an increase in other diseases associated with increased rodent populations (such as hantavirus) may also increase plague here as well. Another pandemic on the scale of the Black Death is unlikely, given that we have improved sanitation, less crowding, and effective antibiotics, but recent outbreaks demonstrate that even a small number of cases can have a huge impact.

Finally, there is the potential to be infected with plague via malfeasance: a terrorist attack. This has been attempted in the past, via the release of Yersinia-infected fleas over Manchuria and China in 1941, or perhaps more famously, the catapulting of corpses who'd died of plague over the walls of the city during the siege of Kaffa by the Tartars in 1347. Today, Yersinia remains a top concern as far as potential bioterrorism pathogens go for a number of reasons. First, unlike anthrax, Y. pestis can be transmitted person-to-person, so any initial outbreak seeded by a terrorist release would spread beyond just the initial exposed group. Additionally, the infectious dose via inhalation is estimated to range from ~100 up to 20,000 organisms, so if it's spread via aerosol by someone who knows what they're doing, it has the potential to cause a lot of damage.

Y. pestis has been a scourge of humanity for centuries. It's shaped our society in a myriad of different ways, and potentially even played a role in shaping our genomes. It may not be a killer of the magnitude of HIV, TB, or malaria, but the swiftness of a plague death and the high mortality rate of those infected means that it remains a threat--and potentially a greater one than it's been in years due to the threat of bioterrorism and expansion of the range of its natural hosts due to climate change and other human factors (such as the crumbling of public health infrastructure and increased contact with rodents due to human encroachment into wildlife areas). The heyday of plague may be hundreds of years in the past, but with infectious diseases, it pays to be ready for the unexpected.

Previous posts in the series

Part 1

Part 2

Part 3

References and further reading

Gubler D. et al. 2001. Climate variability and change in the United States: potential impacts on vector- and rodent-borne diseases. Environ Health Perspect. 109 Suppl 2:223-33. Link.

Stenseth, N.C., Atshabar, B.B., Begon, M., Belmain, S.R., Bertherat, E., Carniel, E., Gage, K.L., Leirs, H., Rahalison, L. (2008). Plague: Past, Present, and Future. PLoS Medicine, 5(1), e3. DOI: 10.1371/journal.pmed.0050003

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Fascinating and informative. Thank you for this series.

Thank you from me as well.

One claim I have read is that the flea which lives on the brown rat is less likely to bite human beings than the species which lives on black rats, and that therefore one reason why bubonic plague is less common is that over the past two centuries the brown rat has ousted the black through much of its range. Is there any evidence for this?

By Maureen Lycaon (not verified) on 23 Jan 2008 #permalink

No--it was originally Pasteurella pestis, then re-named for him later.

Maureen, I'm not sure about the rats. I've heard that as well but I don't have any science to confirm or deny it. I found one paper in PubMed with the title "Is the brown rat (Rattus norvegicus Berkenhout) responsible for the disappearance of plague from Western Europe?" from 1956, but it doesn't even offer an abstract. I'm sure there's something out there that analyzes this in depth, but I'm not familiar with it.

Thank you for the reply. I had no better luck trying to find the paper anywhere online, and it doesn't even seem to have been cited much.

Hopefully, some day someone else will do research into this.

By Maureen Lycaon (not verified) on 24 Jan 2008 #permalink

Who cares about what caused the black plague, we should be more focused on emerging epidemics now. Such as mycoplasma incognitus/penetrans. Nicolson is finding it in 50% of CFS/FIBROmyaligia patients, and its the only microbe out of hepatitis c/hiv that induces disease in experimental animals. The NIH Dr. Joel Baseman on Military scientists Shyh ching Lo's work.

The meeting was led by Dr. Joel B. Baseman, a mycoplasma expert at the University of Texas Health Sciences Center at San Antonio. He said the participants were ''very impressed with the quality of science that Dr. Lo's group displayed.''

''The pathology data was solid and convinced us that the agent is in the tissues,'' Dr. Baseman said. The ability of M. incognitus to cause a fatal wasting disease in monkeys and mice persuaded most participants that the microbe ''has the potential to cause disease in humans,
New York Times 1990.

Could not be a contaminent for Lo saw it in patients tissues by EM. Antibody testing is unreliable, for the monkeys only had a weak response when near death. Researchers from U of Alabama confirmed it was a novel strain when they inoculated rats with it and found to be highly invasive vs the normal strain of MF.

The blood bank isnt safe, there are thouands of people infected with this microbe that are being misdiagnosed as hypochondriacs, Time for you people to stop being denialists and speak out, instead of babbling about ancient history.

Thanks for this series of posts, I did a HS biology term paper on then Y pestis, so it's near and dear to me.

Just off-hand, I think the anthrax hypothesis smells funny. Anthrax has been a long time fellow-traveller with us humans (more specifically, our cattle) for ages, long before the Great Plague. "Murrains" devastated many a ruminant population, and anthrax is not noted for being hghly infectious human to human. So, you would have to posit a mechanism whereby anthrax, which caused a low level of human death pretty much constantly for thousands of years, very suddenly became a virulent, highly infectious pandemic, devastated a continent.. and then went back to being background nastiness.

Also, because anthrax was a background nastiness, finding victims of anthrax concurrent with the plague means next to nothing. Plenty of other diseases would have taken the opportunity to have their own little outbreaks during periods of high societal stress and infrastructure breakdown, too.

Of course, I'm just a history wonk with an interest in biology....

Lab Lemming's comment of a few days ago stimulated my 70yo brain to recall some informal research done in the 50's on Y. pestis in the assorted ground squirrels of the great plains. Also included were several species of voles. I see nothing to rule out lemmings as the vector in Iceland but our relative ignorance. Incidentally, anecdotal records of some reliability suggest a number of suspicious deaths in the Canadian prairie provinces during the 30's might be the result of Y. pestis - acquired by the victims, all older boys and teenagers, from the habit of cutting off the tails of S. richardsonii and sticking them in their pants pockets in order to collect the bounty offerred by local authorities. This was especially puzzling in the case of Alberta, which was - and still is - largely rat free! Doctors with military experience were quick to suggest plague, but predictably, were laughed out of court. No rats, no plague, Right?
All of which simply begs all of these many questions. As long as we know so little about the critters involved, micro and macro, their many and varied serotypes, population dynamics, etc., then so long will we continue these - admittedly interesting - debates. I know of no research - past, present or planned - for comprehensive antibody studies of our native rodents, their commensals and non-rodent acquaintences (Mustellidae, perhaps?) Could be a Ph.D or two here. Keep stimulaating debate, Dr. Smith - we may just learn something yet.

By Ken Waight (not verified) on 28 Jan 2008 #permalink

Great series, Tara. Quick question: what do you think of John Kelly's surmise that marmot plague may be responsible for the particular virulence of certain Y. Pestis outbreaks?

Thanks for putting this series up on the side-bar. I really enjoyed reading it but I missed it the first time around. It's a well written series too. Thanks.

Just come across this series after a couple of days amateur researching the Black Death; easily the most informative, accessible, and fair-minded explanation I have found, which seems compelling and nearly conclusive. Still haven't found much about the black rat/brown rat issue though, and generally what caused catastophic plague events in 541 and 1347, apparently followed by successive waves over centuries until dying back to the endemic source areas.

Anyway, thanks very much indeed!