Category Archives: microbiology

Contours of the Black Death Cemetery at Charterhouse Square, London

Excavations for the Crossrail Extension project discovered the second major Black Death cemetery in London in 2013. This week the first peer-reviewed publication of findings from the site appeared (in press).  As a rescue excavation in the midst of a construction project, the site had to be quickly surveyed for the extent of the cemetery and this is what is contained in this publication.

This site is part of 13 acres leased by Sir Walter de Mauny from St Bartholomew’s Priory for an emergency cemetery for plague victims in 1349 AD.  The site has been used for a variety of purposes over the centuries and currently is a four acre green space called Charterhouse square. The site is graphically displayed below with the locations of later structures.

Crossrails site, London
Crossrails site in Charterhouse Square, London (Dick et al., 2015)

The initial discovery came in a shaft just to the southwest of the Charterhouse Square. There they found three layers of graves with a total of 25 bodies lacking signs of trauma and with pottery shards from 1270-1350 AD. Subsequent radiocarbon dating and aDNA analysis confirmed that they were victims of the Black Death.

The surveys conducted over just two days were able to outline the broad contours of features at the site. These included a 15th century building, a priory kitchen, a probable World War II submerged emergency water tank, and a possible ditch and bank along the cemetery that is mentioned in descriptions. They believe that a disturbed area in the southwest corner represents about 200 individual graves, although only excavation can confirm these graves. They concluded that their ability to detect medieval objects in such an intensely used urban area suggests these methods are a good option for similar future situations.

The scans also revealed some surprises. There are not as many graves as descriptions suggest should have been there, though bodies may be more dense that suggested by the scans. They also did not find any large pits of  stacked bodies. This indicates that even during the height of the Black Death, many people were still buried in individual graves. Graves were found in three phases with layers of clay-rich earth in between perhaps in an attempt to seal the graves. These scans should allow them to target future excavations to areas with a high probability of dense graves.


Dick, H. C., Pringle, J. K., Sloane, B., Carver, J., Haffenden, A., Stephen Porter, H. A., et al. (2015). Detection and characterisation of Black Death burials by multi-proxy geophysical methods. Journal of Archaeological Science, 1–50. doi:10.1016/j.jas.2015.04.010 [In press, accepted manuscript]

An Anniversary year for Natural Disasters: 1815, 1665, and 1315

There are major natural disasters every year. In the last year alone we have had the major earthquake in Nepal just in the last couple days and a historic epidemic of Ebola. It’s too soon to tell how these latest disasters will seen by history and effect historical interpretations. This year there are three natural disaster anniversaries that stand out from the rest not just due to their mortality but also because of their impact on how we interpret the past.

Tambora, 1815

Mount Tambora Volcano, Sumbawa Island, Indonesia
Mount Tambora Volcano, NASA image (public domain)
Just a few weeks ago there was a minor splash in the news to mark the 200th anniversary of the eruption of Tambora on April 5, 1815. The photo to the right is the caldera of Tambora taken from space. As tragic as the thousands of deaths directly related to the eruption are, 1815 is best known as the ‘year without a summer’, a volcanic winter. It is impossible to know how many deaths resulted from crop failures and unseasonable weather. As the most recent volcanic winter, 1815 is an important because we have the most reliable scientific data, economic data, and descriptions of the effects on health and culture from people in all walks of life all over the globe. I don’t know as much about Tambora and its after effects as I would like, so I’m planning on reading The Year Without a Summer by historian William Klingman and meteorologist Nicholas Klingman (2013). If I like it, maybe you will hear more about it later this year.

Great Plague of London, 1665

This year is also the 350th anniversary of the Great London Plague that was followed closely by the Great London fire. Despite its reputation, the great plague of London was not the last major plague of Europe by a long shot.

17th century London
17th century London

The 1665 plague of London claimed up to 100,000 lives, about as many as died in the Marseille plague of 1720-3. Fifty years later, a similar size plague struck Moscow under Empress Catherine the Great. Yet, the London Plague is the one that gets the most attention.

A great deal of the notoriety of the Great Plague of London comes from the amount and quality of resources available in English.  Daniel Dafoe immortalized the plague in his novel, Journal of a Plague Year written in 1722. A savvy author, Dafoe timed it to take advantage of plague fears in southern Europe, concurrent with the plague in Marseille. It is testament to the Dafoe’s skill as a writer than his novel is often taken as historical evidence. I think I’ll mark the anniversary by reading Defoe’s classic.

The London plague has also been magnified by it linkage with the great fire of London in 1666. The relationship between the fire and the plague has been controversial. It has been sometimes assumed that the fire ended the plague, but the plague was winding down before the fire began. However, it is likely that the fire removed the environment that had supported the plague preventing its return; over 80% of the citizens of London were left homeless. Restoration of the capital city after the great fire also immortalized 1665-6 in the history of London.

Great European Famine, 1315

A less combustible but perhaps equally deadly anniversary this year is that of the Great Famine of 1315 that effected most of continental Europe. Seven hundred years ago the famine began and, while its hard to estimate famine mortality over three to seven years, perhaps up to 15% of Northern Europeans died. It began with soaking and then flooding rains that destroyed winter crops for two years with yields of wheat and rye in England and Wales 60% below normal in 1316, and again in 1321 with similar drops in yield. Also beginning in 1315 the great bovine pestilence, possibly rinderpest,  begins in Central Europe and spread across the continent: France and Germany, the Low Countries,  Denmark and England by 1319. In just one year, England and Wales lost approximately 62% of all bovines (Slavin 2012). The loss of dairy and beef was compounded by the fact that oxen provided the vast majority of traction and fertilizer. With similar losses across Europe, it took nearly 25 years to return cattle numbers to the pre-epizootic levels.

There was no respite for the 14th century. The childhood survivors of the famine and food shortage were the adults who were cut down by the Black Death in the 1340s. What effect malnutrition had on their developing immune system is a line of inquiry being explored by anthropologists Sharon DeWitte and historian Philip Slavin (2013). Let us not forget, it still got worse, between the crop failures and panzootic of 1315 and the Black Death in 1346 , the Hundred Years’ War begins in 1337.


Devaux, C. A. (2013). Small Oversights That Led to the Great Plague of Marseille (1720-1723) Lessons From the Past. Infection, Genetics and Evolution, 14(C), 169–185. doi:10.1016/j.meegid.2012.11.016 (for comparisons to other epidemics)

Slavin, P. (2010). The Crisis of the Fourteenth Century Reassessed: Between Ecology and Institutions — Evidence from England (1310-1350). EHA Paper, 1–14.

Slavin, P. (2012). The Great Bovine Pestilence and its economic and environmental consequences in England and Wales, 1318–501. The Economic History Review, 1–28.

Dewitte, S., & Slavin, P. (2013). Between Famine and Death: England on the Eve of the Black Death—Evidence from Paleoepidemiology and Manorial Accounts. Journal of Interdisciplinary History, 1–25.

Plasmodium knowlesi: A New Ancient Malaria Parasite

There are over a hundred different species of the malaria-causing Plasmodium parasites in reptiles, birds and mammals. Being so widespread among terrestrial vertebrates, zoonotic transfer of Plasmodium has come at humans from multiple different sources. Plasmodium knowlesi had been known for some time as a parasite of long-tailed macaques but was not considered a significant human parasite until 2004 when a large number of human infections were identified in Borneo. Molecular analysis implies that Plasmodium knowlesi is as old as Plasmodium vivax and Plasmodium falciparum.

Cover image the phases of Plasmodium knowlesi from the April 2013 issue of Clinical Microbiology Reviews.

Diagnosis is complicated by the histological similarity between Plasmodium knowlesi and Plasmodium malariae. They can’t be distinguished in blood smears like those shown here, so infections were most often misdiagnosed as P. malariae even though they cause a quotidian (daily) fever. The WHO recommends that microscopic detection in areas where P. knowlesi is found report positive results as “P. malariae/P. knowlesi”.  It can only be securely diagnosed by molecular methods  that can distinguish all five human malarial species. PCR based detection methods have shown promise but no one method has been clinically tested with a large enough number of cases to become the standard of care. Antibody-based Rapid Diagnostic Tests (RDT dipstick tests) for malaria do not reliably detect knowlesi malaria which was discovered in humans after the RDT tests were developed. For now in resource poor areas, microscopic analysis followed by molecular testing where available is the only way to detect knowlesi malaria. Clinical research continues for a RDT test that can be employed areas with poor laboratory resources.

Infections have now been confirmed in all of the countries of southeast Asia. Between 2000 and 2011, 881 cases of local P. knowlesi local transmission have been identified in Borneo, with only 8 cases of P. malariae.  It is now suspected that past diagnoses of P. malariae in the region were actually P. knowlesi. Unlike other forms of malaria, P. knowlesi infects more adults than children, although actual infection rates are still not known.

Long-tailed and pig-tailed macaques are the reservoirs for P. knowlesi. In some areas of Malaysia the macaques are around 90% seropositive for malaria, in one study 87% were P. knowlesi. The malaria vector for P. knowlesi and other malarial parasites is Anopheles leucosphyrus group which is also concentrated in southeastern Asia.  Anopheles balabacensis is the most efficient vector, capable of transmitting P. knowlesi from monkey-to-human, human-to-human and human-to-monkey. A. latens, on the other hand, has been most commonly indicated as the vector to humans in Borneo, where it feeds in the high elevation canopy.  As the map below shows, the macacque reservoir and the mosquito vectors are limited to  the islands and peninsulas south-east Asia. It has been hypothesized, based on genetic diversity, that P. knowlesi has caused human malaria as long as  humans, macaques and the Anopheles vectors have all been on the islands of south-east Asia.

Source: Singh, B., & Daneshvar, C. (2013). Human Infections and Detection of Plasmodium knowlesi. Clinical Microbiology Reviews, 26(2), 165–184. doi:10.1128/CMR.00079-12

Difficulty in diagnosis has made it made it challenging to study the full spectrum of knowlesi malaria across the population. What studies have been done show that it produces a full spectrum of malarial disease from mild to fatal. Most cases reported to-date are in adult males, making an occupational exposure a significant possibility.

Symptoms are representative of other malarial infections: fever, chills and rigor, headache, along with a cough, abdominal pain and diarrhea. Gastrointestinal symptoms correlate with high levels of the parasite in the blood. Thrombocytopenia (low platelet counts) is the most common clinical finding and more severe than in either vivax or falciparum malaria, while anemia appears to be mild in knowlesi malaria. In the few pediatric cases that have been observed, they all responded to anti-malarial therapy. In the few cases of severe disease reported, abdominal symptoms have been so severe in some that malaria was not initially suspected. Acute Respiratory Distress Syndrome (ARDS) has been reported in about 50% of severe cases and acute renal failure in approximately 40%. There have not yet been enough confirmed cases of knowlesi malaria to accurately determine the case fatality rate. Although it appears to respond to a wide range of anti-malarial drugs, an optimized treatment based on a sufficient number of cases was not yet available in 2013.

The discovery of Plasmodium knowlesi in humans comes in the context of increasingly successful control of vivax and falciparum malaria in southeastern Asia. Some of the latest epidemiology from Malaysia suggest that 50-60% of the cases of malaria are now knowlesi. There are fears that knowlesi will jeopardize regional malaria elimination efforts. Is the rate really increasing or is it only apparent as levels of falciparum and vivax decrease? Does a real increase represent an opening niche for knowlesi as vivax and falciparum decrease? Only time and more data will answer our questions.

Primary Reference:

Singh, B., & Daneshvar, C. (2013). Human Infections and Detection of Plasmodium knowlesi. Clinical Microbiology Reviews, 26(2), 165–184. doi:10.1128/CMR.00079-12

For additional epidemiology from Malaysia:

Yusof, R., Lau, Y. L., Mahmud, R., Fong, M. Y., Jelip, J., Ngian, H. U., et al. (2014). High proportion of knowlesi malaria in recent malaria cases in Malaysia, Malaria Journal 13(1), 1–9. doi:10.1186/1475-2875-13-168

William, T., Jelip, J., Menon, J., Anderios, F., Mohammad, R., Mohammad, T. A. A., et al. (2014). Changing epidemiology of malaria in Sabah, Malaysia: increasing incidence of Plasmodium knowlesi, Malaria Journal 13(1), 1–11. doi:10.1186/1475-2875-13-390