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.

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.

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References

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. http://doi.org/10.1002/ajpa.20818

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. http://doi.org/10.1537/ase.161011

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. http://doi.org/10.1016/S1473-3099(04)01099-0

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.

Ötzi’s Lyme Disease in Context

One of the ancient DNA finds that continues to intrigue me is the discovery of Borrelia burgdorferi, the agent of Lyme disease, in Ötzi the 5300-year-old ice mummy from the Italian Alps. As far as I know, this is the only finding of B. burgdorferi in ancient remains of any date.  I discussed the initial report of these findings back in the summer of 2012. 

A reconstruction of Oetzi the iceman. (Thilo Parg / Wikimedia Commons; License: CC BY-SA 3.0)

Ixodes ricinus (starved) (Photo: James Lindsey, CC by SA 3.0 via Wikipedia)

 

The more we learn about Ötzi’s environment and lifestyle, the less mysterious it seems. There are no signs of human habitation or land management in these high Alpine regions. Indicators of deforestation, farming, and pasture maintenance are lacking from lake sediment and pollen studies. Festi, Putzer and Oeggl (2013) found the first signs of human land management in the Ötztal Alps to began about 1000 years after Ötzi’s time. During the Copper Age, subsistence occupation of the valley floor was sufficient for the population of Ötzi’s time. They did minimal farming, and breeding of caprines (sheep, goats, and ibex). Festi, Putzer and Oeggl (2013) note that Ötzi’s mummy is the only piece of evidence for humans that high in the Otztal Alps before the Bronze Age.

Before Ötzi’s time, landscape management in the Mesolithic was to support red deer herds that were “in a state of semi-domestication by means of active hunting” (Rollo et al, 2002). (Native Americans managed deer populations in similar ways by promoting a landscape where deer thrive near their hunting grounds.) The importance of deer to Ötzi is underscored by everything about him from the red deer meat in his stomach to the roe deerskin that made up his quiver and antler in some of his tools (Rollo et al, 2012). Two different species of deer have been confirmed by genetic analysis.  Most of his clothing was made of sheep and goat skins (O’Sullivan et al, 2016).

The agent of Lyme disease, B. burgdorferi, is transmitted primarily by the tick Ixodes ricinus, common on deer, sheep, cattle, humans and dogs as adults and feed on rodents and small mammals as nymphs. Ticks often thrive at the forest edge where there are grasses for them to climb up to catch passing deer. It seems likely that they would also thrive in along upland forest edges as well. Ixodes ricinus is found throughout the Alps.  It is feasible that Lyme disease was a greater problem for humans when we relied on deer as a staple food.

Ötzi’s B. burgdorferi has yet to be confirmed by a second group. Interestingly, a recent study of B. burgdorferi’s phylogeny suggests that it originated in Europe and later spread to ‘post-Columbian’ North America (Margos et al, 2008). Although Lyme disease was only recognized in the 20th century, it is apparently an ancient disease caused by multiple Borrelia species. And Ötzi’s sequence has not been added to any phylogeny I’ve found, odd. Overlooked, or a problematic sequence?

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References

Festi, D., Putzer, A., & Oeggl, K. (2013). Mid and late Holocene land-use changes in the Otztal Alps, territory of the Neolithic Iceman “Otzi”. Quaternary International, 353, 1–18. http://doi.org/10.1016/j.quaint.2013.07.052

Margos, G., Gatewood, A. G., Aanensen, D. M., Hanincová, K., Terekhova, D., Vollmer, S. A., et al. (2008). MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proceedings of the National Academy of Sciences, 105(25), 8730–8735. http://doi.org/10.1073/pnas.0800323105

O’Sullivan, N. J., Teasdale, M. D., Mattiangeli, V., Maixner, F., Pinhasi, R., Bradley, D. G., & Zink, A. (2016). A whole mitochondria analysis of the Tyrolean Iceman’s leather provides insights into the animal sources of Copper Age clothing. Scientific Reports, 6, 1–9. http://doi.org/10.1038/srep31279

Rollo, F., Ubaldi, M., Ermini, L., & Marota, I. (2002). Otzi’s last meals: DNA analysis of the intestinal content of the Neolithic glacier mummy from the Alps. Proceedings of the National Academy of Sciences of the United States of America, 99(20), 12594–12599. http://doi.org/10.1073/pnas.192184599

Early use of the term ‘malaria’

I was reading Robert Sallares’ Malaria and Rome this evening and I noticed some information on the earliest use of the term ‘malaria’ that I thought would be worth sharing.

As we have all learned, malaria comes from the Italian mal’ aria, meaning ‘bad air’. A few other interesting facts:

• Marco Cornaro’s books Scitture della laguna  published in Venice in 1440 is the earliest use of the term mal aere.
• Horace Walpole was the first to introduce the word malaria to English literature in his Letters in 1740 : “There is a horrid thing called malaria, that comes to Rome every summer, and kills one” (p. 9).
• Guido Baccelli’s La malaria di Roma, published in 1878, is the first application of the term specifically to the disease.

Does anyone know of earlier uses of the term?

Source: Robert Sallares, Malaria and Rome: A History of malaria in ancient Italy. Oxford University Press, 2002.