Historians/History

The Shifting Explanations for the Black Death, the Most Devastating Plague in Human History

by John Kelly

Mr. Kelly, who holds a graduate degree in European history, is the author most recently of The Great Mortality: An Intimate History of the Black Death, The Most Devastating Plague of All Time (HarperCollins), from which the following article is adapted.

FOR THE LAST TWENTY YEARS, A SMALL BUT VOCAL GROUP OF scholars has been challenging the traditional view of the Black Death as a plague pandemic. The “origins” controversy, as it might be called, was ignited in 1984 when Graham Twigg, a respected British zoologist, published The Black Death: A Biological Reappraisal. Since then, works such as The Biology of Plagues, by Susan Scott, a British sociologist, and her colleague, biologist Christopher J. Duncan; and The Black Death Transformed, by Samuel K. Cohn, a professor of medieval history at the University of Glasgow, have kept the controversy roiling. For lack of a better term, these authors—and their supporters—might be called the Plague Deniers, since they believe that the Black Death was caused by a disease other than plague.

The Deniers’ case against Y. pestis can be reduced to two basic points. The first and weaker part of their argument involves their pet theories about what else could have caused the medieval plague. Anthrax, zoologist Twigg’s candidate, has never struck a human community in epidemic form and does not produce buboes (although anthrax victims do develop black boils). Professor Cohn’s candidate is a mysterious Disease X, which he does not name, but believes has probably gone extinct. Scott and Duncan go furthest of all, arguing improbably that many of the worst epidemics in Western history, from the fifth century B.C. Plague of Athens to the Black Death, were caused by an by an Ebola-like illness they call hemorrhagic plague.

The second part of the Deniers’ case against Y. pestis is far more substantial. Our modern understanding of plague is based on the comprehensive studies that were done during the Third Pandemic. In the hinge decades between the nineteenth and twentieth centuries, Alexandre Yersin identified the plague bacillus; Paul-Louis Simond, a French scientist, the rat-flea mechanism that drives the disease; and the Indian Plague Commission, a creation of the British Raj and one of the great achievements of Victorian medicine, compiled an unprecedentedly detailed profile of Y. pestis. Commission officials studied the role climate, sanitation, population density, and—in a few commission reports—nutritional status played in the spread of the plague bacillus and its vectors, the rat and rat flea. The commissioners also looked at which transportation facilities and goods were most often associated with the movement of the disease—grain unsurprisingly proved to be a big magnet for rats.

As the Plague Deniers are quick to point out, the disease that emerged from the commission’s findings bears little resemblance to the disease described in the Black Death chronicles. A case in point already mentioned is the widely different dissemination rates of the two pandemics. While the Black Death virtually leaped across Europe, sometimes traveling two to two and a half miles a day, the plague of the Third Pandemic moved at a relatively sluggish ten to twenty miles per year. Another key difference is the astonishing variation in mortality rates. How could a disease that killed at least a third of the population in one appearance (the Black Death) kill under 3 percent of the population in a later outing? Some of the other discrepancies the Plague Deniers cite include:

• Differences in symptoms. Cardinal Francis Aidan Gasquet, the great Victorian scholar of the Black Death in England, was among the first experts to call attention to this difference. Writing at the time of the Third Pandemic, the cardinal noted that contemporary accounts of the “ordinary eastern or bubonic plague” rarely mentioned four symptoms that Black Death chroniclers referred to frequently. The four were: a “(1) Gangrenous inflammation of the throat and lungs, (2) violent pains in the region of the chest, (3) vomiting and spitting of blood, and (4) the pestial odor coming from the bodies and breath of the sick.”

Add contagion to the cardinal’s list of symptoms, and you have an almost perfect description of the disease Friar Michele da Piazza described tumbling off the Genoese galleys at Messina. “Breath spread the infection . . . , and it seemed as if victims were struck all at once by the affliction . . . and so to speak, shattered by it. . . . [They] violently coughed up blood and after three days of incessant vomiting for which there was no cure, they died.”

Louis Heyligen’s description of the Black Death also contains the cardinal’s symptom list. “The disease is threefold in its infection,” Heyligen wrote,” . . . firstly men suffer in their lungs and breathing, and whoever have these corrupted or even slightly attacked cannot by any means escape nor live beyond two days. . . . Many dead bodies have been . . . dissected and it is found that all that die, thus . . . have had their lungs infected and spat blood. . . .”

Echoing Cardinal Gasquet, the Plague Deniers note that no description of the Third Pandemic, whether written by the Indian Plague Commission or by other Western scientists, contains a list of symptoms comparable to that of Friar Michele and Heyligen, and that includes the symptom of contagion, since until it goes pneumonic, modern plague is spread via rat and flea, not from person to person.

Descriptions of the bubo do appear in accounts of both the Third Pandemic and the Black Death. But as Professor Cohn, a leading Plague Denier, notes, medieval and modern accounts of the plague describe the bubo differently. In modern plague, 55 to 75 percent of the time, the bubo develops in the groin, 10 to 20 percent of the time in the neck. Since the ankle is the most flea-accessible part of the body, this pattern makes sense. However, it is not the pattern described by many Black Death chroniclers. Fourteenth-century accounts usually locate the bubo higher up on the body, behind the ears, for instance, or on the throat, regions difficult for an insect to reach, even one that can jump one hundred times its height.

• Rat die-offs. Since the rat flea, X. cheopis, does not jump to humans until the local rat population is nearly obliterated, in theory an outbreak of human plague should be preceded by a large rat die-off. And during the Third Pandemic, practice usually followed theory. Preplague rat die-offs were common. However, references to them are exceedingly rare in the literature of the Black Death. Some scholars have tried to explain away the omission by claiming that dead rats were so common on the medieval street, chroniclers thought them unworthy of mention. To put it charitably, that theory seems improbable in the extreme. If an epidemic on the scale of the Black Death was caused by a rat-borne plague, the streets would have been knee-deep in dead rats and people would have noticed and written about that.

• Incidence of pneumonic plague. The disease described by Friar Michele, Louis Heyligen, and other medieval chroniclers sounds like a variant of pneumonic plague, and, judging from the frequent references to blood spitting and hypercontagiousness in early accounts of the plague, the pneumonic disease seems to have been very common in the first six to twelve months of the Black Death, even in regions where the climate should have been hostile to it, like the Mediterranean south. In contrast, in modern outbreaks of the disease, pneumonic plague is uncommon. Some scholars claim that as many as 15 to 25 percent of modern plague cases “go pneumonic.” But in Vietnam only 2 percent of the reported cases did.

• Climate. The whole issue of climate and plague is perplexing. Plague outbreaks during the Third Pandemic usually reflected the sensitivities of the rat and flea vectors. Outbreaks were rare during the Indian hot season, when the weather was very hot and dry, but common on either side of the hot season, when humidity increased and temperatures moderated—creating conditions favorable to X. cheopis. By contrast, the Black Death seemed to be largely immune to climatic effects. While outbreaks were slightly more common in warm weather, as Plague Deniers Scott and Duncan note, in some regions of Europe the mortality reached its peak in December and January. Indeed, Y. pestis killed almost as many people in frigid Greenland as it did in temperate Siena.

Before turning to the rejoinders of what might be called the Plague Defenders, a group that includes the majority of historians and almost all microbiologists, mention should be made of two recent discoveries by a team of French scientists. Diagnosing a disease from a list of symptoms in a medieval chronicle or medical tract—a favorite strategy of the Plague Deniers—is fraught with difficulties and imprecisions. One doctor’s carbuncle can be another’s plague boil. More fundamentally, written evidence ignores the fact that diseases, like people, often change over time. Measles and syphilis look and behave a lot differently today than they did when they first burst into the European population.

DNA is a far more trustworthy diagnostic tool. With that thought in mind, in the late 1990s a group of French paleomicrobiologists removed dental pulp from corpses buried in two plague pits in southern France and tested it. One pit dated from the Black Death, the other from a later recurrence of the plague. In a series of papers published in the Proceedings of the National Academy of Sciences, the French investigators reported finding DNA from Y. pestis in both samples. The French work has yet to be confirmed by researchers in other laboratories—the final step in scientific acceptance—but Didier Raoult, the lead investigator in the DNA study, is confident of his team’s findings. The “medieval Black Death was the plague,” he says without equivocation.

But what kind of plague?

Adopting the Russian view and describing the Black Death as an outbreak of marmot plague would help to explain many of the discrepancies that trouble the Plague Deniers. For example, marmot plague’s tropism for the lungs would account for the seemingly high incidence of pneumonic disease—even in warm climates, where the weather would not have favored its transmission. Moreover, marmot plague is the only form of rodent plague that is contagious; marmots spread the disease the way humans do, via a marmot version of the cough.

Of course, marmot plague is still marmot plague. But if Dr. Wendy Orent is correct, and at some point the marmot disease evolved into a distinctly human form, given its genetic heritage, such a “humanized” plague might well produce symptoms like chest pain, blood spitting, and, as the lungs and throat became gangrenous and corrupted, a fetid body and breath odor. A humanized version of Y. pestis would also explain the absence of rat die-offs. Such an ailment would spread the way Friar Michele and Louis Heyligen describe the Black Death spreading, directly from person to person by way of the breath, though very likely other modes of transmission would have also developed. Thus, Dr. Orent thinks that P. irritans, the human flea, would have played an important role in the spread of a “humanized” plague.

Like their Russian counterparts, many American microbiologists reject the arguments of the Plague Deniers, but for different reasons. Most American scientists do not accept the Russian theory of “host” plague strains—that is, that the lethality of a particular strain of Y. pestis is shaped by its evolutionary history with particular rodent species. The plague bacillus is only fifteen thousand to twenty thousand years old, says Professor Robert Brubaker, dean of American plague researchers. In evolutionary terms, Dr. Brubaker thinks that is not enough time for the bacillus to have evolved very far away from its original form.

In Dr. Brubaker’s view and that of most of his colleagues, the Black Death and the Third Pandemic were classic examples of rat-borne plague. In the American view, differences between the two outbreaks can be explained largely in terms of external factors. One of the most important of these externals is the very different levels of knowledge available to physicians of the fourteenth and late nineteenth centuries. From firsthand observation, medieval Europeans sensed that plague was affected by factors like sanitation, nutrition, and the movement of goods and people, but this practical knowledge was attached to beliefs about the importance of astrology, miasmas, and bodily humors.

“By the late nineteenth century,” says Dr. Brubaker, “physicians and scientists understood the principles of contagion . . . [and] had a good working knowledge of how infectious disease spreads and the measures needed to be taken to safeguard public health.” One by-product of this new understanding was that seven-hundred-year-old insights could now be transformed into effective public health strategies. The municipal health board of Black Death Florence may have had little success with its sanitary measures, but “the Indian Plague Commissioners believed that they were able to prevent catastrophe [by] imposing aggressive controls on public and hospital sanitation,” says historian and physician Ann Carmichael of the University of Indiana.

Effective sanitary measures also played an important role in controlling plague outbreaks in Hong Kong and Canton in the mid-1890s. However, in those localities, physicians cited two other measures with Black Death echoes as also important—adequate nutrition and decent nursing care.

It is noteworthy that when measures like stringent sanitation collapsed, as happened in Bombay during a disease outbreak in 1897, the plague of the Third Pandemic quickly began to behave like the plague of the Black Death. In a Bombay hospital a plague commissioner characterized as rife with “fatigue, destitution, filth, poverty and overcrowding,” the death rate reached 64.5 percent in the spring of 1897. Professor Cohn may be correct in saying that no outbreak of the Third Pandemic produced mortalities on the scale of the Black Death, but in the terrible months between August 1896 and February 1897, Bombay lost nineteen thousand people to the disease.

A modern understanding of another aspect of sanitation—personal hygiene—may also help explain why, if the Black Death was an outbreak of rat plague, there were so few rat die-offs. Given the unhygienic state of the medieval body, it is highly likely that P. irritans, which preys on people, not rodents, played a major role in spreading the plague from person to person.

The Plague Deniers have long argued that P. irritans’s bite, unlike X. cheopis’s, transmits too few plague bacilli to make it a very efficient disease vector. However, that weakness may not have mattered during the Black Death. Whatever its form, the medieval plague was extraordinarily virulent; the very high concentrations of bacilli in human blood may have turned even normally weak insect vectors into efficient plague carriers. Furthermore, it is not at all clear that the human flea is that weak a disease vector. Observers as diverse as General Ishii (inventor of the Japanese plague bomb), United States Army Intelligence, and Giovanni Boccaccio have all offered testimonials to P. irritans’s efficiency as a disease carrier. The two pigs Boccaccio describes as dropping dead after mauling a blanket almost certainly were killed by the bite of P. irritans, which is a pig as well as human flea.

Perhaps the most compelling testimony about the effectiveness of the human flea as a plague vector comes from Dr. Kenneth Gage, chief of the Plague Division at the Centers for Disease Control. From his personal experience fighting the disease in modern Africa, Asia, and South America, Dr. Gage has become convinced that the human flea plays an important but underappreciated role in the spread of plague.

The weakest part of the Black-Death-as-a-purely-rat-borne-plague theory involves the apparently very high incidence of the pneumonic form of the disease. Secondary pneumonic infections occur in bubonic plague, but, at least in modern experience, only infrequently. French scholar Jean-Noël Biraben hypothesizes that the unusually cold weather of the fourteenth century may have been especially “pneumonic-friendly.” The problem with the Biraben theory is that, south of the Alps, the weather was still warm when the Black Death arrived.

One possible explanation for the high rate of “pneumonic” Black Death is that two disease strains were at work in 1348 and l349. The Manchurian outbreak of pneumonic plague in 1911 arose from marmots. Yet the epidemic occurred in the midst of the rat-based bubonic plague of the Third Pandemic. Perhaps something similar occurred during the Black Death? Another possibility is that over the course of the middle years of the fourteenth century, Y. pestis underwent a fundamental evolutionary change, as Dr. Orent suggests.

Medievalist and physician Ann Carmichael also has a theory about the medieval plague, one that addresses not only the high incidence of pneumonic disease but, more sweepingly, why, on many clinical and epidemiological indexes, it looks so different from the Third Pandemic. “There may have been something fundamentally different about the nature of the premodern world,” says Dr. Carmichael, “something we don’t understand and which cannot be duplicated today even in Third World regions.”

However, about one thing we can be certain.

Microbiologist Didier Raoult is right; the Black Death was an outbreak of plague.