Category Archives: bioarchaeology

Pregnancy, ‘coffin birth’, and the Black Death

by Michelle Ziegler

The Genoese have always been central in the legend of the start of the Black Death, by their own claim, linking a siege of the Genoese at Kaffa to the spread of the epidemic in the Mediterranean. Last month the first confirmed plague graves in the region of Genoa were reported by Cesana, Benedictow, and Bianucci in the cemetery of the ospitali (hospital) of San Nicolo. The hospital of San Nicolo was located at a node along the route connecting the hilly backcountry of Genoa to the main travel routes of medieval Italy.

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Fetus skeleton. Only fragments were found of the skulls and pelvises for all four individuals. (Cesana, Benedictow, & Bianucci, 2017)

The quadruple grave consisted of a woman in her 30s with full-term fetus in the birth canal (a ‘coffin birth’), and two children aged approximately 3 and 12 years, based on their growth and tooth eruption. Dated stratigraphically to the second half of the 14th century, they are a very rare multiple grave for Northern Italy. No plague pits have been discovered in this region.

They were screened for plague with the RDT dipstick (here and here) that detects the F1 antigen of Yersinia pestis (see also Bianucci et al, 2008 and Pusch et al, 2004). This test has proven quite reliable for archaeological material and is a useful tool for modern diagnosis in resource-poor areas. The RDT dipstick is a more sensitive test than aDNA so we should not expect every positive skeleton by the RDT to produce aDNA but it is a good screening tool prior to aDNA surveys and useful for epidemiological purposes. The adult female, the fetus and the oldest child all gave positive results by the RDT dipstick. I would consider these to be positive plague cases with or without aDNA confirmation. Now I do have one caveat at this point, I’m not ready to assume that the fetus is a true positive, although it is certainly possible. Since it was present in a decaying maternal body with lots of F1 antigen around, the protein could have been absorbed into the fetal bones during the decomposition process. If there is enough aDNA to be detected and readable in the fetal bones, then I would consider it a stronger case.  Regardless, the plague was at least the secondary cause of death for the fetus since it claimed the life of its mother.   Without more genetic testing, we will not know the relationship between the two older children and the woman. They could be one family, although at a hospital they could be of no relation to each other.

Without a more precise date or ancient DNA, we can not predict which plague epidemic produced this grave. Raffaella Bianucci has informed me that these graves will be part of a large aDNA project currently underway, so more information will be available eventually. Then the historical analysis of Ole Benedictow in this article will be very helpful in placing them in a more precise context.

My main interest lies with the pregnant plague victim and her fetus. A coffin birth is caused by the build up of gasses in the corpse that pushes the fetus out of the birth canal. Given that plague victims die of septicemia, possibly infecting the placenta, it’s not all that surprising (at least to me).

Given a high medieval birth rate, I am surprised that more pregnant women have not been found in plague graves. Stephen Ell (1989)  found that 8.5% of all women between ages 15 and 50 were reported as pregnant in the death records he analyzed for three days in an October 1630 epidemic in Venice.    So why haven’t fetuses or newborns been found in more plague graves?

There are a few possible reasons for fewer fetuses than expected: early pregnancies are unlikely to leave fetal bones, and in a stacked mass grave, tiny fetal bones would easily get jumbled with all the other bone bits. When fetal bones are found in these mass burials it may be difficult to determine how many fetuses they represent.  Reports from the third pandemic and later may provide a few more clues.

So let’s look at a parallel late-term pregnancy infection from 1975 (Welty et al, 1985, 641-2): a 31-year-old Navajo Arizona woman in her 9th month of pregnancy presented at a clinic with a high fever, headache and a tender right axillary node whose aspirate produced the bipolar safety pin looking bacillus suggestive of Yersinia pestis. This was later confirmed by culture and she was started on Streptomycin. On the first day of admission, the baby’s heart rate was already at 200 beats per minute suggesting fetal distress so she was induced, and she delivered a healthy baby boy.  His cord blood was negative for plague and he never developed a plague antibody titer. Two days later the mother’s two and a half-year-old child was admitted with a fever (104 F), cough, headache, and vomiting. Her axial lymph nodes were also positive for Yersinia pestis and she was started on antibiotics as well. All three were recovering well when released from the hospital nine days after the mother’s original admission.

Clearly, antibiotics and the ability to induce the birth made all the difference in this case. The placental blood barrier seems to have held just long enough for a healthy delivery. In the few other cases in the literature, antibiotic treatment appears to rescue the pregnancy, although induction of delivery is recommended if there are signs of fetal distress at 36 weeks of gestation or later. The pre-antibiotic scenario is much grimmer:

“In the preantimicrobial era, plague reguarly resulted in abortion, and the aborted tissues were occasionally infected with plague bacillus. In 1903 Jennings reported 10,000 cases of plague, 14 of which occurred during pregnancy. Four of the mothers survived, but spontaneous abortions or still births occurred in 13 of the patients, including the four survivors. One of the 14 patients was near her expected date of delivery. The child was born apparently well, but the mother died of postpartum hemorrhage. Ten hours after birth, lymphadenopathy was noted in the infant’s groins and axillae and it died one day later.” (Welty et al, 1985, 645)

In another case report from 1975, Mann and Maskowitz (1977) opined that “fetal wastage resulting from a maternal infection with plague probably results from the systemic effects of illness rather than direct placental or fetal infection, although true intrauterine infection with plague as been described.”  Fetal distress detected in the case described above and in the other case reported by Mann and Moskowitz both support a risk to the pregnancy prior to fetal infection. Infection of the fetus and/or placenta would have been a very grave development without access to antibiotics. I can not imagine how a maternal immune system could clear such an infection. At any rate, it seems likely that most infected pregnant women lost their fetus to miscarriage or stillbirth prior to their own death. This would account for a lower than expected number of pregnant women found in plague burials. Given that fetuses and infants are underrepresented in normal cemeteries, it is possible that many of these unbaptized infants in plague times were not buried with the rest of the community.

All of the modern cases would have been managed slightly differently today. The Navaho woman’s entire family would have been examined and given antibiotics immediately. It is hard to believe today they waited until the two-year-old had a 104-degree fever before being examined. Modern plague management guidelines have detailed instructions for treating pregnant women for bubonic and pneumonic plague to maximize safety and limit side effects of the drugs on the fetus (Inglesby et al, 2000). However, saving the mother’s life trumps all considerations if ideal antibiotics are not available or working sufficiently. Prior to 36 weeks of gestation when it can be induced, this is also the best chance the fetus has for survival.


Bianucci, R., Rahalison, L., Massa, E. R., Peluso, A., Ferroglio, E., & Signoli, M. (2008). Technical note: a rapid diagnostic test detects plague in ancient human remains: an example of the interaction between archeological and biological approaches (southeastern France, 16th-18th centuries). American Journal of Physical Anthropology, 136(3), 361–367.

CESANA, D., BENEDICTOW, O. J., & Bianucci, R. (2017). The origin and early spread of the Black Death in Italy: first evidence of plague victims from 14th-century Liguria (northern Italy). Anthropological Science, 1–10.

Ell, S. R. (1989). Three days in October of 1630: detailed examination of mortality during an early modern plague epidemic in Venice. Reviews of Infectious Diseases, 11(1), 128–141.

Inglesby, T. V., Dennis, D. T., Henderson, D. A., Bartlett, J. G., Ascher, M. S., Eitzen, E., et al. (2000). Plague as a biological weapon: medical and public health management. Working Group on Civilian Biodefense (Vol. 283, pp. 2281–2290). Presented at the JAMA : the journal of the American Medical Association.

Mann, J. M., & Moskowitz, R. (1977). Plague and pregnancy. A case report. Jama, 237(17), 1854–1855.

Pusch, C. M., Rahalison, L., Blin, N., Nicholson, G. J., & Czarnetzki, A. (2004). Yersinial F1 antigen and the cause of Black Death. The Lancet Infectious Diseases, 4(8), 484–485.

Welty, T. K., Grabman, J., Kompare, E., Wood, G., Welty, E., Van Duzen, J., et al. (1985). Nineteen cases of plague in Arizona. A spectrum including ecthyma gangrenosum due to plague and plague in pregnancy. The Western Journal of Medicine, 142(5), 641–646.

Presentations on the Plague from the European Association of Archaeologists, Vilnius, Lithuania, 2016

I just discovered that most of the presentations from the “Plague in Diachronic and Interdisciplinary Perspective” session of the Europan Association of Archaeologists meeting in Vilnius, Lithuania on 2 September 2016 are now on YouTube.  I think I have collected them all here. Enjoy 3 hours of plague talks!

Introduction-Plague in diachronic and Interdisciplinary perspective by Marcel Keller

From Mild to Murderous: How Yersinia pestis Evolved to Cause Pneumonic Plague by Wyndham Lathem (30 min)

Reconstructing ancient pathogens – discovery of Yersinia pestis in Eurasia 5,000 Years Ago by Simon Rasmussen (15 min)

Plague in the eastern Mediterranean region 1200-1000 BC? by Lars Walloe (15 min)

Placing the Plague of Justinian in the Yersinia pestis phylogenetic context by Jennifer Klunk (15 min)

A demographic history of the plague bacillus revealed through ancient Yersinia pestis genomes by Maria Spyrou (15 min)

Analysis of a High-coverage Yersinia pestis Genome from a 6th Century Justinianic Plague Victim by Michal Feldman (15 min)

Early medieval burials of plague victims: examples from Aschheim and Altenerding (Bavaria, Germany) by Doris Gutsmiedl-Schumann (15 min)

Fleas, rats and other stories – The palaeoecology of the Black Death by Eva Panagiotakopulu (15 min)

Plague in Valencia, 546: A Case Study of the Integration of Texts and Archaeology by Henry Gruber (15 min)

Germany and the Black Death: a zooarchaeological approach by M.A. Paxinos

Evolutionary Clues in 17th-Century Smallpox Genome

By Michelle Ziegler

Smallpox is one of those diseases long believed to have an ancient pedigree, the suspected culprit of legendary epidemics. Yet, so far, smallpox hasn’t made a big impression in ancient DNA surveys. If it was truly endemic throughout the Old World before 1492, so much so that it pops up in the New World almost immediately after contact, it’s odd that it has not been more prominent in ancient DNA surveys. Be ready for a smallpox paradigm shift and reexamination of its reputed history.

In December, Ana Duggan, Maria Perdomo, and the McMaster Ancient DNA Centre team announced the first full ancient smallpox genome isolated from a mummified 17th-century child in Vilnius, Lithuania. Radiocarbon dates of the child place him or her in the mid 17th century (est. c. 1654) in the midst of dated smallpox epidemics from all over Europe.

Fig 1 (Duggan et al, 2016): Left: Distribution of smallpox records in Europe. Right upper: Dominican Church of the Holy Spirit, Vilnius. Lithuania. Right lower: Crypt containing the child’s remains.

Their finding was unexpected. They were not looking for smallpox at all; the child had no observable lesions. They were hoping to find JC polyomavirus, of particular interest to one of the co-authors, and so they first enriched the specimen for this virus (McKenna 2016). After detecting variola virus (VARV), smallpox, instead they then enriched for VARV to confirm the initial signal.

duggan_cbsmallpox_finalMore than just confirming the signal, they were able to reconstruct the entire genome producing the entire sequence at an average depth of 18X. The surprising child had more revelations in his or her viral sequence. The sequence is ancestral to all existing reference strains. This is consistent with short stretches of aDNA amplified from 300-year-old frozen Siberian remains (Biagini et al, 2012). Unfortunately, the sequences from 2012 were not distinctive enough from the new Lithuanian sequence to give phylogicial resolution between them. Oddly, the frozen Siberian remains also lacked smallpox skin lesions with one showing signs of pulmonary hemorrhages.

Its ancestral position in the phylogeny suggests that a severe bottleneck occurred before c. 1654. As Duggan et al (2016) remark, vaccination would cause a very strong bottleneck, but this occurs after 1654 and there is new diversity among the descendent reference specimens producing two major clades. Yet to be determined is the evolutionary effect of extensive variolation practices in the early modern period. In contrast to vaccination, variolation is a form of intentional smallpox transmission that sometimes went horribly wrong.

Evolution continues unabated. The molecular clock is consistent among the 20th-century specimens and the latest aDNA from the Lithuanian child. The two clades of smallpox collected from 20th-century specimens diverged from each other sometime around the mid-17th century after vaccination began. Interestingly, the less virulent Variola minor strain is not predicted to have emerged from Variola major clade P-II until the mid-19th century.

Evolutionary history of Variola (Duggan et al, 2016)

It’s not entirely surprising that smallpox, a highly transmissive human-only virus, has a relatively recent last common ancestor; other viruses like measles do as well. Measles last common ancestor is probably in the early 20th century (Furuse, Suzuki & Oshitani, 2010). The dominance of the 1918 influenza strain in recent influenza phylogeny is another example; incomplete because influenza swaps genes with influenza viruses that are circulating primarily in birds, but also in swine and earlier in equines (Taubenberger & Morens, 2005). Improved transmission strains are likely to out-compete strains with a lower transmission rate if they achieve a global spread. For some viruses, though not necessarily all, improved transmissibility and virulence go hand in hand. So, in the end, the relatively recent last common ancestor says more about its global transmissibility than anything else.

The antiquity of the virus needs two components to estimate. The molecular clock must be steady, and it is so far (though this could change with more ancient specimens), and a near relative ‘out group’, related strains outside the Variola clade (a branch of the larger genetic tree). One potential problem here is that as transmissibility improves the clock may speed up. The speed of the clock is determined by the reproduction rate. The relatively steady clock back to this 17th-century specimen suggests that the transmission rate was pretty steady — after the evolutionary/transmission leap that swept aside other Variola strains. The inactivation of several orthopoxvirus genes in smallpox that are functional in vaccinia (used in smallpox vaccines), camelpox, and taterapox  (the ‘out groups’ used) may suggest that one or more of these genes had been protective. When the genes were inactivated, smallpox probably became a much more dangerous virus to humans.

Historical epidemiology suggests that there was once more variation in the virulence of smallpox epidemics.  Securely identifying smallpox epidemics in the historical record is much harder than is generally assumed, and it is harder yet to make a claim for a significant demographic impact prior to the Renaissance (Carmichael & Silverman, 1987). This is the problem with theories that smallpox was the cause of the second-century Antonine plague and then failed to cause an epidemic with a major demographic effect for many centuries. I find this very hard to believe. Additionally, the infamous smallpox epidemics in the New World are now also be reevaluated in ways that diminish smallpox’s toll and add in a wide variety of contributing factors to produce a colonization syndemic. This has most recently been summarized in essays collected in Beyond Germs: Native Depopulation in North America (2015).

One other observation from these studies: All ancient smallpox DNA to date has been extracted from mummy tissue, not a tooth or bone. This may point toward one of the limitations of ancient DNA pathogen surveys that currently use primarily teeth. Since neither mummy had visible smallpox lesions, smallpox should be considered a possibility in any mummy.


Duggan, A. T., Perdomo, M. F., Piombino-Mascali, D., Marciniak, S., Poinar, D., Emery, M. V., et al. (2016). 17th Century Variola Virus Reveals the Recent History of Smallpox. Current Biology, 1–7.

Biagini, P., Thèves, C., Balaresque, P., Géraut, A., Cannet, C., Keyser, C., et al. (2012). Variola virus in a 300-year-old Siberian mummy. The New England Journal of Medicine, 367(21), 2057–2059.

McKenna, Maryn (8 Dec 2016) Child Mummy Found with Oldest Known Smallpox Virus. National Geographic. (online)

Carmichael, A. G., & Silverstein, A. M. (1987). Smallpox in Europe before the seventeenth century: virulent killer or benign disease? Journal of the History of Medicine and Allied Sciences, 42(2), 147–168.

Furuse Y, Suzuki A, & Oshitani H (2010). Origin of measles virus: divergence from rinderpest virus between the 11th and 12th centuries. Virology journal, 7 PMID: 20202190

Taubenberger, J. K., & Morens, D. M. (2005). 1918 Influenza: the mother of all pandemics. Emerging Infectious Diseases, 12(1), 15–22.

Beyond Germs: Native Depopulation in North America. Edited by Catherine Cameron, Paul Kelton, and Alan Swedlund. University of Arizona Press, 2015.