Category Archives: Black Death

Changing the Plague-Flea Transmission Paradigm

The old paradigm is dead! Long live the new paradigm!

X. cheopis, the rat flea
Xenopsylla cheopis, the rat flea

Rebecca Eisen, David Dennis, and Kenneth Gage just published an article gathering all the evidence that should put an end to the blocked flea model  as the only significant method of plague transmission.  They summarize the data proving that unblocked fleas can and do transmit Yersinia pestis at levels that readily cause infection in rodents and humans. They call all transmission by unblocked fleas early phase transmission (EPT), even in flea species that never block.

Important findings summarized:

  • The blocked flea model –  that only a biofilm blocked Xenopsylla cheopis which can not eat so it tries to aggressively feed and  regurgitates high numbers of Yersinia pestis into the bite site – is insufficient to account for either epizootics or large human outbreaks. Blocked fleas do transmit the plague but are simply insufficient to account for the speed and volume of epizootic and epidemic transmission.
  • Transmission can occur as quickly as the very next blood meal taken by the flea, at times within 1-2 hours. Y. pestis does not need to replicate in the flea for transmission to occur. This makes it much more likely that the flea will survive long enough to transmit the infection.
  • Early phase transmission has been experimentally observed to cause infections after exposure to a single Oropsylla montana flea. Therefore, exposure to large numbers of unblocked infected fleas is not required for transmission. Epidemiologic findings suggest that most US cases come from bites from a single or at most a few fleas, and this is consistent with findings around the world were fleas that do not block are primary vectors.
  • Many reservoirs of plague are maintained by fleas that never block. Prairie dog reservoirs in the western US and great gerbil reservoirs in central Asia are both maintained by fleas that are never blocked by a biofilm.
  • “In short, EPT was observed in all flea species evaluated at varying temperatures. Transmission occasionally occurred as early as 3 h post-infection but usually was observed over 1-4 dpi [days post infection]. Although all flea species tested were capable of EPT, efficiency in these studies varied among species, suggesting that some fleas are likely to be more important than others in the rapid spread of plague in nature, especially those that are both efficient transmitters and abundant on susceptible hosts.” (p. 3)

  • Strains of Y. pestis that can not form a biofilm transmit as effectively by EPT as biofilm competent strains. Virulence factors that are necessary for biofilm production are not necessary for EPT.
  • EPT – compared to a contaminated “dirty needle” – is a mechanical form of transmission that “requires no modification or multiplication of the pathogen in the vector for transmission to occur” (p. 4).
  • In the pre-antibiotic era, many human bubonic plague infections and all septicemic and pneumonic cases would have produced bacteremia levels sufficient to infect fleas for EPT. In the 71 fatal plague cases recorded by the CDC between 1956 and 2013, 86.8% were either primary or secondary septicemic cases.
  •  “Epidemic support in favor of interhuman flea borne transmission comes from records of limited bubonic plague outbreaks in isolated rural communities under exceptional circumstances of heavy human flea infestations, high familial attack rates, and a lack of evidence for concurrent rat-flea borne plague. … [studies in Africa, the Middle East and the Andes mentioned]… Based on epidemiologic pattern of person to person spread, especially the high attack rates among contacts of the sick, an absence of domestic rats, and an unusual abundance of P. irritans infesting villages and their homes, investigators concluded that the outbreak resulted from infective bites by P. irritans.” (p. 7-8)

  • They note that interhuman plague transmission by pulex irritans has been documented early in the 20th century and supported by laboratory experiments. As covered here a year ago, infected Pulex irritans were recovered from the homes of plague patients in Madagascar in 2013. They end with a call for more work on P. irritans to evaluate its role in modern and historical human epidemics.

It is worth noting here that throughout the article they cite many studies using many different fleas. EPT studies have also been demonstrated  for mouse fleas (Aetheca wagneri Baker)  and cat fleas (Ctenocephalides felis).  I’ve never really understood why studies of historic plagues often overlook mice as a source of fleas.

I also have to add that mechanical transmission by the flea makes a lot of evolutionary sense.  It gives evolution a place to start tinkering. ‘Good enough’ is the stuff of evolution! Optimization only occurs after a very long evolutionary process, and may never be achieved. The fact that X. choepis evolved a method (via bioflim blockage and regurgitation [LPT]) to keep transmission going longer does suggest that the rat flea has been historically important to Y. pestis evolution. Obviously mechanical transmission has also allowed Y. pestis to expand into areas and exploit new opportunities where a more complicated, required transmission system would have been an obstacle.

Experiments proving that EPT is possible have been scattered over the last 50 years! And, yet the old paradigm still reigned. Why? Obviously there has been a lack of communication within science and between science and the humanities. It would really be helpful for a historian of 20th century science to look into how this could have happened.


Eisen, R. J., Dennis, D. T., & Gage, K. L. (2015). The Role of Early-Phase Transmission in the Spread of Yersinia pestis. Journal of Medical Entomology, tjv128–10. Advanced access, Aug. 19, 2015. (Open access)

Spring Reading

It has been a busy spring. I haven’t had a chance to blog as much as I would have liked to, but I have done quite a bit of reading. Some of my reading has been on the complex world of the first plague pandemic. To say that it was transformative would be an understatement.  One of the social questions for the first plague pandemic is how does plague and other natural disasters effect a population that is the midst of conversion?  When the Black Death came it encountered a fully Christian and Muslim world, but not so during the first pandemic. Most of Europe was not yet Christian in 541. There were some Jews, Christians of several varieties, Roman pagans, Germanic pagans, Celtic pagans, Zoroastrians, North African and Middle Eastern pagans, etc. Yet at the end of the pandemic period, Islam is born (and fast growing) and Christianity is dominant in Europe (and united by Rome). The plague began in a polytheistic world and ended in a monotheistic one. What role did the plague play, if any? Yet to be determined. This really isn’t a peripheral issue. Every writer of the first pandemic was involved in this transformation (winners and losers) in some way and it effected how they wrote about the plague and other calamities. So I have a lot of reading to do; below is a start and a few other things that caught my attention.


Marilyn Dunn. (2010) The Christianization of the Anglo-Saxons, c. 497- c.700: Discourses of Life, Death and Afterlife.

Marilyn Dunn (2013) Belief and Religion in Barbarian Europe, c. 350-700. Bloomsbury.

Peter Brown (2015) The Ransom of the Soul: Afterlife and Wealth in Early Christianity. Harvard University Press.

Peter Heather (2013) The Restoration of Rome: Barbarian Popes and Imperial Pretenders. Oxford University Press.


Balbir Singh and Cyrus Saneshvar (2013) Human Infections and Detection of Plasmodium knowlesi. Clinical Microbiology Reviews. 26 (2): 165-184.

Runfola, J. K., House, J., Miller, L., Coltron, L., Hite, D., Hawley, A., et al. (2015). Outbreak of Human Pneumonic Plague with Dog-to-Human and Possible Human-to-Human Transmission — Colorado, June–July 2014. MMWR. Morbidity and Mortality Weekly Report, 64(16), 429–434.

Smith-Guzmán, N. E. (2015). Cribra orbitalia in the ancient Nile Valley and its connection to malaria. International Journal of Paleopathology, 10, 1–12. doi:10.1016/j.ijpp.2015.03.001

Benovitz, N. (2014). The Justinianic plague: evidence from the dated Greek epitaphs of Byzantine Palestine and Arabia. Journal of Roman Archaeology. doi:10.1016/S1473-3099(13)70323-2)

Bernard Bachrach, (2007) Plague, Population, and Economy in Merovingian Gaul. Journal of the Australian Early Medieval Association. 3: 29-57.

Sarris, P. (2002). The Justinianic plague: origins and effects. Continuity and Change, 17(02), 169–182. doi:10.1017/S0268416002004137

Newfield, T. P. (2015). Human–Bovine Plagues in the Early Middle Ages. Journal of Interdisciplinary History, 46(1), 1–38. doi:10.1179/146141010X12640787648612

Inskip, S. A., Taylor, G. M., Zakrzewski, S. R., Mays, S. A., Pike, A. W. G., Llewellyn, G., et al. (2015). Osteological, Biomolecular and Geochemical Examination of an Early Anglo-Saxon Case of Lepromatous Leprosy. PLoS ONE, 10(5), e0124282. doi:10.1371/journal.pone.0124282.s001

Shanks, G. D., & White, N. J. (2013). The activation of vivax malaria hypnozoites by infectious diseases. The Lancet Infectious Diseases, 13(10), 900–906. doi:10.1016/S1473-3099(13)70095-1

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

Lowell, J. L., Antolin, M. F., Andersen, G. L., Hu, P., Stokowski, R. P., & Gage, K. L. (2015). Single-Nucleotide Polymorphisms Reveal Spatial Diversity Among Clones of Yersinia pestis During Plague Outbreaks in Colorado and the Western United States. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), 15(5), 291–302. doi:10.1089/vbz.2014.1714

Neil, B. (2013). The Papacy in the Age of Gregory the Great. A Companion to Gregory the Great, 3–28.

Brogiolo, G. P. (2015). Flooding in Northern Italy during the Early Middle Ages: resilience and adaption. Post-Classical Archaeologies, 5, 47–68.

Kostick, C., & Ludlow, F. (2015). The dating of volcanic events and their impact upon European society, 400-800 CE. Post-Classical Archaeologies.  5, 7–30.

Riehm, J. M., Projahn, M., Vogler, A. J., Rajerison, M., Andersen, G., Hall, C. M., et al. (2015). Diverse Genotypes of Yersinia pestis Caused Plague in Madagascar in 2007. PLoS Neglected Tropical Diseases, 9(6), e0003844. doi:10.1371/journal.pntd.0003844.s002

Makundi, R. H., Massawe, A. W., Borremans, B., Laudisoit, A., & Katakweba, A. (2015). We are connected: flea–host association networks in the plague outbreak focus in the Rift Valley, northern Tanzania. Wildlife Research, 42(2), 196. doi:10.1071/WR14254

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]