Category Archives: anthropology

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 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 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

War as a Driver in Tuberculosis Evolution

by Michelle Ziegler

Russia has been all over the news lately. Beyond our recent election, increased Russian activity on the world stage has public health consequences for Europe and farther afield. It has been known for a long time that post-Soviet Russia had and continues to have serious public health problems. One of their particular problems that they have shared with the world is their alarmingly high rate of antibiotic resistant tuberculosis. There is no mystery over the root cause of their antibiotic resistance woes — poor antibiotic stewardship (Garrett, 2000; Bernard et al 2013).

A study by Vegard Eldholm and colleagues that came out this fall sheds light on the origins of particularly virulent tuberculosis strains with high rates of antibiotic resistance that recently entered Europe.  A large outbreak among Afghan refugees and Norwegians in Oslo, Norway, provided a core set of 26 specimens for this study that could be compared with results generated elsewhere in Europe (Eldholm et al, 2010). The Oslo outbreak clearly fits within the Russian clade A group that is concentrated to the east of the Volga River in countries of the former Soviet Union. They name this cluster the Central Asian Clade, noting that it co-localizes with region of origin of migrants carrying the MDR strains of tuberculosis reported in Europe.

Figure 5. Phylogeny of the Afghan Strain Family (ASF). Colored boxes represent the country of origin: Afghanistan is orange; other countries are gray. (Eldholm et al, 2016)

When the Oslo samples are added to the family tree, phylogeny, of recent tuberculosis isolates from elsewhere in Europe a distinctive pattern emerges. The branches on the family tree are short and dense, suggesting that this is recent diversity, that they calculate to have occurred within approximately the last twenty years (Eldholm et al, 2016).

The Central Asian Clade spread into Afghanistan before drug resistance began to develop, probably during the Soviet-Afghan war (1979-1989) producing the Afghan Strain Diversity clade. Slightly later, the Central Asian Clade still in the former Soviet states begins to accumulate antibiotic resistance as the public health infrastructure crumbles in the wake of the dissolution of the USSR. The invasion of Afghanistan by the US and its allies in 2002 toppled the Afghan state, crippling infrastructure and spurring refugee movements within and out of Afghanistan. The lack of modern public health standards in Afghanistan since their war with the introduction of these strains by the Soviets in the 1980s provided fertile ground for the establishment and diversity of tuberculosis in the country. Instability has been pervasive throughout the entire region sending refugees and economic migrants from both Afghanistan and the former Soviet states into Europe.

Movements of the Central Asian Clade (CAC) since c. 1960 and the subsequent Afghan Strain Family (ASF). (Eldholm et al, 2016)

Their dating of the last common ancestor for the Central Asian Clade to c. 1961 is significantly younger than the previous dating of 4,415 years before present for the Russian clade A (CC1) of the Beijing lineage of Mycobacteria tuberculosis. They account for this difference by noting differences in their methods of assessing sequence differences and note that their method is in line with other recent evolutionary rates for other tuberculosis clades.  The diagnosis dates and length of the arms on their reconstructed phylogeny suggests that there were multiple, independent introductions of the cases from Afghanistan and the former Soviet republics. This is consistent with a repeated periods of refugee movements from central Asia into Europe.

The rapid proliferation and diversification of the Afghan Strain Family may be explained by a known syndemic between tuberculosis and war (Ostrach & Singer, 2013). Conditions of war everywhere disrupt food systems, destroy critical infrastructures such as electricity and water systems, interrupts medical supplies, and the human public health infrastructure of the country. Malnutrition and stress are known contributors to immune suppression. Many pathogens flourish simultaneously in these conditions increasing the infectious challenges the population must fend off. Diarrheal diseases are the most acute and demanding of rapid attention, allowing longer-term diseases like tuberculosis to slip through the overburdened healthcare system. Afghanistan has experienced nearly forty years of war, political instability, and repeated infrastructure destruction. Thus, they were primed for both the establishment of new tuberculosis strains during the Afghan-Soviet war in the 1980s along with the proliferation and diversification of tuberculosis during the Afghan-American war of the last sixteen years.

Established syndemics between tuberculosis and war have been made retrospectively following the Vietnam war and the Persian Gulf war of 1991 (Ostrach & Singer, 2013). In Vietnam, prolonged malnutrition caused an eruption of tuberculosis along with malaria, leprosy, typhoid, cholera, plague, and parasitic diseases.  A WHO survey in 1976 found that Vietnam had twice the incidence of tuberculosis over all of its neighboring countries (Ostrach & Singer, 2013). When the military intentionally targets water infrastructure as it did in Vietnam and Iraq, the production of civilian infectious disease is a tactic of war. In both Vietnam and post-Gulf war Iraq, more civilians died of malnutrition and infectious disease than enemy soldiers died of all causes (Ostrach & Singler, 2013).

It seems likely that this is just one of the first studies to establish a link between serious infectious disease developments and the Afghan wars. The current war zones throughout central Asia and the Middle East already have ramifications for the public health of the entire world that walls along borders will not be able to stop. Most of the cases in the Oslo outbreak were Norwegians, not Afghan immigrants. Diseases will spread beyond the migrants so country of origin screening will be of little use before long.


Eldholm, V., Pettersson, J. H. O., Brynildsrud, O. B., Kitchen, A., Rasmussen, E. M., Lillebaek, T., et al. (2016). Armed conflict and population displacement as drivers of the evolution and dispersal of Mycobacterium tuberculosis. Proceedings of the National Academy of Sciences of the United States of America, 201611283–16.

Ostrach, B., & Singer, M. C. (2013). Syndemics of War: Malnutrition-Infectious Disease Interactions and the Unintended Health Consequences of Intentional War Policies. Annals of Anthropological Practice, 36(2), 257–273.

Bernard, C., Brossier, F., Sougakoff, W., Veziris, N., Frechet-Jachym, M., Metivier, N., et al. (2013). A surge of MDR and XDR tuberculosis in France among patients born in the Former Soviet Union. Euro Surveillance: Bulletin Européen Sur Les Maladies Transmissibles = European Communicable Disease Bulletin, 18(33), 20555.