The besieged need bread In May of 1590, the city of Paris came under siege. France was in the throes of the wars of religion, and the city was held by the supporters of the ultra-Catholic "Holy League." Henri III, the last of the Valois kings, had been assassinated in 1589, and his heir was Henri of Navarre, a Protestant, whose accession the leaders of the League were determined to resist.1 Henri of Navarre moved to enforce his claim to the throne by force of arms, and on May 7th, his troops began to advance on Paris.2 The siege of Paris (along with much that led up to and followed it) was chronicled in the diary of one Pierre de L'Estoile, clerk-in-chief of the French Parlement. It is to his Memoires-Journaux that we owe the account of a strange experiment (reminiscent of the giant in the story "Jack and the Beanstalk") in the making of bread from human bones. It quickly became obvious that existing stores of food were inadequate to feed the population during a lengthy siege. In mid-June, an assembly was called "to find a way to deal with the famine which was growing from day to day in Paris."3 At this assembly, it was proposed that the bones of dead Parisians stored in the charnel house at the Cemetery of the Innocents be ground into flour and baked into bread for the "nourishment of those who had no grain and no way to get any."4 Bizarre as the proposal seems, L'Estoile notes that "not a man in the assembly was found to oppose" it.5 This plan was duly put into action, and, by August 16th (by which time the poor had descended to eating dogs, cats, tallow and grass),6 L'Estoile reported that "the bread made of the bones of our fathers ... began to be used."7 This experiment in quasi-cannibalism, however, proved to be a resounding failure; L'Estoile adds in the same journal entry that the use of the bone-bread "didn't last long because those who ate it died."8 Of course, it is possible that L'Estoile was in error as regards the universal lethality of the bone-bread, which was baked specifically for "those who had no grain and no way to get any."9 L'Estoile was a member of a more affluent class for whom food was still available, although at an exorbitant price.10 For this reason, it is unlikely that L'Estoile knew personally any of those who consumed the "bread," so it may be that some people did indeed eat it and live to tell the tale. Assuming that L'Estoile's information was correct, however, we are left with a puzzle: Why should eating "bread" made of ground bones prove fatal? Or, put another way, what was the causative agent in the deaths of those who ate it? This paper represents an admittedly unscientific attempt to unravel this riddle. In the course of considering this mystery of the lethal bone-bread, several hypotheses presented themselves. These hypotheses, with the evidence and arguments for and against them, are examined below. As a prelude to this examination, however, it will be useful to consider the source of the bones in question. The Cemetery of the Innocents, from which the bones were taken, was situated on the right bank of the Seine, next to the marketplace of les Halles.11 Like many other medieval cemeteries, the Innocents practiced a form of grave-recycling; because cemeteries tended to fill up over the course of the centuries, older graves were "regularly reopened and emptied to make way for more burials."12 The disinterred bones were then stored or "charnelled" in a specially-built structure called a charnel house, or charnier. These charnel houses took different forms in different cemeteries, but the one in the Cemetery of the Innocents consisted of a series of arcades surrounding the open area of the cemetery. These arcades (whose lower sections "were mostly given over to family shrines")13 "were roofed with an attic storey, in which exhumed bones were stored. This storey was open under the eaves, and had open skylights or dormers, to allow air to circulate, and the piled-up skulls and bones were clearly visible. Bones had been stored in this way since at least the fourteenth century, and it remained one of the most remarked features of the Innocents ..."14 It was this charnier that supplied the bones used to make the lethal "bread" of 1590. Having established the provenance of the bones, we now turn to a consideration of how and why "bread" made from those bones killed those who ate it. Hypothesis #1:

The deaths were psychogenic, caused by the violation of the near-universal taboo against cannibalism. This hypothesis appeared improbable for three reasons. First, there are many records of people facing starvation who resorted to cannibalism without subsequently dying psychogenic (or "self-willed") deaths; these instances include those of some Donner Party members15 and of Jean-Baptiste-Henri Savigny, who survived the wreck of the French ship La Meduse in 1816.16 Secondly, psychogenic deaths as described in the medical and anthropological literatures tend to be caused by the belief that one is the victim of witchcraft or a curse, rather than the knowledge that one has violated a taboo. (In "'Voodoo' Death," the seminal article on the subject, Walter Bradford Cannon does mention a Maori woman who died within hours of discovering that she had eaten fruit "taken from a tabooed place"; in that case, however, the woman stated specifically "that the sanctity of the chief had been profaned and that his spirit would kill her ...")17 Finally, and most tellingly, L'Estoile notes that certain members of the clergy told their parishioners that "it was better to kill one's own children, and even to eat them raw, than to give in to a heretic ..."18 Given the religious establishment's open endorsement of infanticide for the purpose of cannibalism, it seems unlikely that the quasi-cannibalism of eating "bread" made from ancient (and anonymous) human bones would have a psychological impact sufficient to cause psychogenic death.

Hypothesis #2:

Some or all of the bones used to make the "bread" came from plague victims (or victims of other diseases) and were contaminated by pathogenic microorganisms. At first blush, this hypothesis seemed reasonable; certainly most modern people would view the eating of the dead as unhygienic as well as ethically distasteful. Closer investigation, however, indicated that this hypothesis was less tenable than appeared at first. It must be remembered that the bones in question were decades (perhaps centuries) old; the bones had been disinterred some years after burial and subsequently stored in an elevated charnier that was partially open to the air. Most microorganisms could not survive under these conditions for an extended period of time. The relatively fragile measles virus, for instance, can survive outside a living host for less than two hours;19 tuberculosis bacilli can survive in dust for up to 120 days and in sputum for as long as eight months;20 and yersinia pestis, the causative agent of bubonic plague, can survive in dead bodies for up to 270 days.21 However, even 270 days is a far cry from the years that would have passed between burial and the bones' conversion into "bread." Furthermore, even if any microorganisms had remained on or in the bones, they would then have had to survive the heat of the ovens used to bake the bone-bread. Given these considerations, it seems improbable that pathogenic microorganisms caused the deaths of those who ate it.

Hypothesis #3:

Some of the bones used to make the "bread" were contaminated by prions, thereby causing variant Creutzfeldt-Jakob Disease (or another, similar transmissible spongiform encephalopathy) in those who ate it. This hypothesis seemed unlikely on several grounds. It is true that transmissible spongiform encephalopathies can be spread by cannibalism (in the case of kuru)22 or by exposure to infected bonemeal (in the case of bovine transmissible encephalopathy or BSE).23 It is also true that prions can survive "years of burial"24 and temperatures much higher than those likely to have been reached in 16th-century bread ovens.25 On the other hand, the variant form of Creutzfeldt-Jakob disease seems to have arisen in the 20th century26 and sporadic, non-variant CJD is extremely rare, with an incidence of about one case per million people.27 Although we do not know how many charnelled bones were ground and baked into "bread," the chances are therefore almost infinitesimal that any of the bones came from CJD victims. Furthermore, it's not clear that everyone who ingests food containing prions inevitably develops a prion-mediated disease. (In fact, it seems almost certain that, during the "mad cow" epidemic of the 1990s, many more Britons ate contaminated meat than actually developed vCJD.) Most tellingly of all, however, the transmissible spongiform encephalopathies have an incubation period of months or even years.28 However, it is clear from L'Estoile's narrative that death ensued fairly quickly after the consumption of the bone-bread; the citizens of Paris would not have observed that "those who ate it died" had there been a lag time of months or years between consumption and death. This seemed effectively to rule out the TSE hypothesis.

Hypothesis #4:

Some of the bones used contained arsenic, which was retained in the "bread" and rendered it toxic. This hypothesis seemed more promising at first glance than it did upon closer examination. It is true that arsenic (the use of which as a poison certainly predates the period in question)29 can be deposited in the bones of those who ingest it.30 It is also true that the lethal dose of arsenic in adults is very small — 120-200 mg.,31 or approximately five one-thousandths of an ounce.32 On the other hand, there are significant problems with this hypothesis. First, although it is impossible to know whether any of the bones ground and baked into "bread" were those of poisoning victims, it seems unlikely that a significant number would fall into this category. The odds against many of the bones' containing arsenic are made still longer by the fact that victims of acute arsenic poisoning who receive large doses die within hours;33 in these cases, there presumably would be no opportunity for the arsenic to be deposited to the bones. Finally, a certain amount of ingested arsenic is excreted in the urine, and additional quantities are sequestered in the liver, spleen, kidneys, and gastrointestinal tracts,34 so, even in cases of chronic arsenic poisoning, only a portion of the lethal dose would be available for deposit to the bones. Given all of this, even if we assume that some of the charnelled bones were those of poisoning victims (or contained trace amounts of arsenic obtained from environmental sources), it is highly unlikely that the total quantity retained in the bones would yield enough arsenic to render the resulting "bread" lethal to everyone who ate it.

Hypothesis #5:

The grinding process yielded small, sharp fragments of bone which, when they were baked into "bread" and eaten, perforated the intestines of those who ate it. This hypothesis appeared much more promising than the preceding five. Most people are aware of the risks entailed in consuming sharp objects, and it is a truism that bones (particularly types that splinter readily, such as chicken bones) should not be eaten by people or by pets. And there are certainly cases in the medical literature of intestinal perforations caused by bones or parts of bones, chicken and fish bones being the most frequent culprits.35 On the other hand, there are objections to the hypothesis as well. For one thing, the bones in question were ground into "flour" before being ingested; while medieval milling methods and technologies were significantly different than modern ones,36 millers in the period were able to produce a relatively fine flour.37 If the bones were sufficiently finely ground, the chance of their containing sharp splinters would presumably be reduced. A second objection arose from an examination of current U.S. laws on the processing of meat products. Under Title 9, Section 319 of the Code of Federal Regulations, up to 20% of the meat portion of foods such as hotdogs, Vienna sausages, bologna,38 "luncheon meat,"39 chili,40 tamales,41 spaghetti sauce with meat and/or meatballs,42 etc., may consist of a product described as "Mechanically Separated (Species) (with "species" being beef, pork, etc.).43 Per Section 319.5 of the Code, mechanically separated (species) may contain up to 3% bone fragments.44 The section on mechanically separated (species) further states that "At least 98 percent of the bone particles present in such product shall have a maximum size no greater than 0.5 millimeter in their greatest dimension and there shall be no bone particles larger than 0.85 millimeter in their greatest dimension."45 In other words, consumers of the products listed above are regularly ingesting bone fragments — presumably without fatal outcomes.

Hypothesis #6:

Because bones are composed primarily of minerals, they offer no significant value in terms of calories or nutrients; those who ate the "bread" obtained no nutritional benefit from it and ultimately died of starvation. This hypothesis proved considerably more promising than some of the others that had been advanced. Approximately 70% of human bone mass consists of inorganic minerals, primarily calcium and phosphate;46 as bone matures, "the inorganic matrix becomes primarily crystalline hydroxyapatite, although sodium, magnesium, citrate, and fluoride may also be present."47 Of the remainder of the bone, approximately 20% is composed of organic molecules (mostly collagen),48 and another 8-10% is made up of water.49 While inorganic minerals such as calcium are a crucial component of the human diet, they contain no calories. This means that the only nutritional value to be gained from the bones would have lain in the little collagen they contained — presuming even that the collagen remained intact in bones that were, as in this case, decades or centuries old. While estimates of minimum caloric intake requirements vary depending on the source (the U.S. Department of Health and Human Services and the U.S. Department of Agriculture list 2,400 calories per day as the recommended requirement for sedentary adult males;50 other authorities, such as the World Health Organization, offer different figures), a diet consisting solely of bones or bone products would fail to meet even the lowest of the standards. "Bread" made from ground bones — while it might have filled the stomach and temporarily allayed the pangs of hunger — would have been essentially useless from a nutritional standpoint. Given this, it is certainly possible that those who ate the bone-bread simply succumbed to starvation.

Hypothesis #7:

Because bones are composed primarily of minerals, the "bread" could be neither digested nor easily excreted once eaten; it accumulated in the gastrointestinal tracts of those who ate it, resulting in fatal intestinal obstructions. Investigation of this hypothesis yielded significant evidence in its support. There are numerous reports in the medical literature of intestinal obstructions arising as a result of pica (the compulsive ingestion of non-food substances such as clay, hair, talcum powder, ashes, etc.)51, 52 Perhaps the strongest evidence for the intestinal-obstruction theory, however, is provided by anthropologist Berthold Laufer's intensive study of geophagia (the eating of soil, clay, etc.). Laufer notes that, in many cultures, these substances have been ingested specifically as remedies for diarrhea, which would imply that they have a constipating effect; the ethnic groups using these mineral substances as anti-diarrheals included various Siberian and Tunguskan tribes, Sumatrans, and aboriginal groups in Australia.53 Laufer's book includes several historical accounts of the use of mineral products as food during times of famine; significantly, these attempts, like the Parisian experiment in making bread from bones, usually had fatal results. When famine struck China's Shan-tung province in 1876-77, for instance, flour was made of pulverized soapstone, but those who consumed it experienced "a terrible constipation which entailed death."54 Earlier famines in China also drove people to subsist partly or wholly on mineral products; a Chinese writer who described the practice noted that "Excessive eating of earth will cause obstructions and evil effects, and will ultimately lead to death ...Those who escape death owe it to the fact that they had mixed other things with the clay."55 Laufer also reports fatal outcomes from the consumption (in central Asia) of bread made from powdered plaster56 and (in Saxony) from "a fossil flour,"57 although the deaths in these cases are not specifically attributed to constipation or "obstructions." Bones, as noted above, are composed primarily of inorganic minerals; therefore, it seems likely that bread made from ground bones would affect the human gastrointestinal system in much the same fashion as bread made from powdered soapstone or other mineral products. If so — if the ingestion of an essentially all-mineral "food" did indeed result in intestinal obstructions — then the lethality of the Parisian bone-bread is adequately explained. Intestinal obstruction, which occurs when the movement of material through the gastrointestinal tract is blocked, generally requires surgery unless the obstruction is only a partial one58; today, even with surgery, the mortality rate is 10% for obstructions of the small intestine and 20% for obstructions of the large intestine.59 Surgical intervention, of course, would not have been an option in 16th-century France, so it seems likely that intestinal obstructions would have proved fatal in most or all instances. Given this, intestinal obstructions must be considered as prime suspects in the deaths of the unfortunate consumers of this grisly "bread". A Curious Postscript The siege of Paris was lifted on August 30th, 1590,60 but the "Holy League" continued to resist the accession of Henri of Navarre, even when he offered to convert to Catholicism. The leaders of the League finally overreached themselves, however, when they convened a meeting of the Paris Estates-General and proposed "electing" the Infanta of Spain (a granddaughter of Henry II of France) to rule the Kingdom in place of Henri. The members of the Estates-General responded with horror to this suggested violation of the time-honored Salic Law, and flatly refused to accept the Infanta as their ruler.61 It might be preferable to starve, or even to kill and eat one's own children, rather than accepting a heretic king — but apparently even submitting to a heretic king was preferable to being ruled by a woman.