The Case for Louse-Transmitted Plague

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Louse illustration by Robert Hooke, Micrographia, 1667. (Public domain)

by Michelle Ziegler

The key to understanding plague — past, present, and future — has always been understanding its vector dynamics. By the latest tally, there are 269 known flea species, plus a small collection of ticks and lice, that can be infected with Yersinia pestis. With this many infected parasites, it’s not a surprise that 344 hosts have been identified (Dubyanskiy & Yeszhanov, 2016), but this list is still incomplete. (It does not include all of the minor hosts in North America.) Regardless, this is not a description of a picky pathogen! Unfortunately, it is far easier to identify infected hosts and potential vectors than to determine which of these insects are effective vectors and their transmission dynamics.

Numerous species of fleas have been identified as plague vectors in specific localities. However, only five infected potential human vectors are possibly involved in a wide distribution of human plague cases — the rat flea Xenopsylla cheopis, the cat flea Ctenocephalides felis, the human flea Pulex irritans,  the human body louse Pediculus humanus humanus, and the human head louse Pediculus humanus capitis. The rat flea and the cat flea are known vectors, but they are unlikely to account for the full transmission of the massive first and second pandemics.  I recently discussed the possible role of the human flea. Given the worldwide distribution of human lice, they are attractive vectors but there is still work to do before they can be considered likely primary vectors for human to human transmission during the first two pandemics.

Raoult Makes his Case…again

Didier Raoult and his team have been working on plague and their louse transmission hypothesis for a long time.  It has already been ten years since they had enough information to write their first review article putting forth their human ectoparasite theory of plague transmission (Drancourt, Houhamdi, & Raoult, 2006).

At this point, their primary supporting evidence was some experiments with human louse plague transmission in rabbits (Houhamdi et al, 2006) and they thought they could associate louse transmission with an “Orientalis-like” biovar of Yersinia pestis they identified in the first two pandemics (Drancourt et al, 2004).  However, later ancient DNA work showed that the first two pandemics were caused by strains of Yersinia pestis that emerged before the Orientalis biovar. Genetic reclassification of Yersinia pestis has also made the biovars largely obsolete.  Tensions between groups working on ancient plague DNA developed quickly, and have been documented by historians Lester Little (2011) and Jim Bolton (2013).

This summer Didier Raoult (2016) restated his “personal view” on the role of lice in plague transmission. This essay is unusual not only as a first person narrative in science, including individual claims of discovery but also for being so vindictive in its attack on his rivals. Again, see Little (2011) and Bolton (2013) for less biased accounts.  His team has done very impressive work.

His team has continued to assemble much of the work needed to argue that human lice were instrumental in at least some of the major human outbreaks of plague during the first two pandemics. Combing primarily French medical reports in North Africa, they were able to identify observations that suggest that lice were involved in some mid-twentieth century outbreaks (Raoult, 2016; Malak, Bitam, & Drancourt, 2016).  One of their most interesting findings in 2011 was the discovery of co-infection with Yersinia pestis and Bartonella quintana (trench fever) in late medieval French remains (Tran et al, 2011).  Trench fever is well known to be transmitted by the human louse. Both B. quintana and Y. pestis have been found in contemporary lice taken from plague patients in regions of endemic plague in the Congo (Piarroux et al, 2013; Drali et al, 2015). Unfortunately, neither of these studies mention the presence or absence of fleas.  That blood feeding lice would be infected is not a surprise, but the question of transmission stubbornly remains. There has yet to be a contemporary outbreak where all potential vectors, fleas and lice, were investigated. On a side note, the finding of widespread B. quintana is interesting, and perhaps a proxy for heavy lice infestation.

Modeling Transmission

In the meantime, while Raoult’s latest summary was in press, additional evidence was beginning to be revealed. Graduate student Katharine Dean of the MedPlag project in Oslo was modeling past epidemics for transmission by rat fleas, human lice, and pneumonic transmission. In her master’s thesis, she showed that lice transmission fits the second pandemic epidemics at Givry in 1348, London in 1563-64, and Florence in 1630-31 better than rat fleas or pneumonic transmission (Dean 2015). At the most recent Yersinia meeting in October, Dean presented a poster with expanded data finding outbreaks that fit each of these three modes of transmission (pneumonic in Manchuria, rat fleas in Sydney and Hong Kong, and lice in many locations) (Dean et al, 2016). Their work is still in progress and I’m sure many will be eager to see their results in due course.

Almost there

There are still a few lingering things to nail down. A modern outbreak investigation that looks at all ectoparasites, fleas and lice,  in the region that suggests lice are involved. It would be good to find lice (or fleas for that matter) in a plague burial that yields Y pestis aDNA. Alternatively, detection of more coinfection of Y. pestis with a louse-transmitted infection like B. quintana would lend additional support.  These findings will require some good fortune. To differentiate between the human flea and lice, a better understanding of the pathology of a Y. pestis infection in the potential vector and its transmission dynamics is really needed. The models can’t differentiate human ectoparasites without more information.

Human ectoparasites are beginning to look much more likely especially for northern epidemics (Hufthammer & Walløe, 2013). More information is still needed to distinguish between human fleas and lice, although they may be both involved in different outbreaks.  We need to be ready for yet another paradigm change in plague history. Looking at the overall plague vector dynamics of the great pandemics, from a sylvatic reservoir to distant human populations, is going to get a whole lot more complicated but also more interesting.


Reference:

Bolton, J. L. (2013). Looking for Yersinia pestis: Scientists, Historians, and the Black Death. The Fifteenth Century, XII, 15–38.

Dean, K. R. (2015, June 1). Modeling plague transmission in Medieval European cities. (B. V. Schmid, Supervisor). Oslo. [Master’s Thesis]

Dean, K. R., Stenseth, N. C., Walløe, L., Lingærde, O. C., Bramanti, B., & Schmid, B. V. (2016, October). Human ectoparasites spread plague during the Black Death and Second Pandemic. Yersinia 12th International Symposium. Tbilisi, Georgia.

Drali, R., Shako, J. C., Davoust, B., Diatta, G., & Raoult, D. (2015). A New Clade of African Body and Head Lice Infected by Bartonella quintana and Yersinia pestis–Democratic Republic of the Congo. American Journal of Tropical Medicine and Hygiene, 93(5), 990–993. http://doi.org/10.4269/ajtmh.14-0686

Drancourt, M., Houhamdi, L., & Raoult, D. (2006). Yersinia pestis as a telluric, human ectoparasite-borne organism. The Lancet Infectious Diseases, 6(4), 234–241. http://doi.org/10.1016/S1473-3099(06)70438-8

Drancourt, M., Roux, V., Dang, L. V., Tran-Hung, L., Castex, D., Chenal-Francisque, V., Ogata, H., Fournier, P-E., Crubezy, E, and  Raoult, D. (2004). Genotyping, Orientalis-like Yersinia pestis, and plague pandemics. Emerging Infectious Diseases, 10(9), 1585–1592. http://doi.org/10.3201/eid1009.030933

Dubyanskiy, V. M., & Yeszhanov, A. B. (2016). Ecology of Yersinia pestis and the Epidemiology of Plague. Yersinia Pestis: Retrospective and Perspective, 918(Chapter 5), 101–170. http://doi.org/10.1007/978-94-024-0890-4_5

Houhamdi, L., Lepidi, H., Drancourt, M., & Raoult, D. (2006). Experimental model to evaluate the human body louse as a vector of plague. The Journal of Infectious Diseases, 194(11), 1589–1596. http://doi.org/10.1086/508995

Hufthammer, A. K., & Walløe, L. (2013). Rats cannot have been intermediate hosts for Yersinia pestis during medieval plague epidemics in Northern Europe. Journal of Archaeological Science, 40(4), 1752–1759. http://doi.org/10.1016/j.jas.2012.12.007

Little, L. K. (2011). Plague Historians in Lab Coats. Past & Present, 213(1), 267–290. http://doi.org/10.1093/pastj/gtr014

Malek, M. A., Bitam, I., & Drancourt, M. (2016). Plague in Arab Maghreb, 1940–2015: A Review. Frontiers in Public Health, 4, 18–6. http://doi.org/10.3389/fpubh.2016.00112

Piarroux, R., Abedi, A. A., Shako, J. C., Kebela, B., Karhemere, S., Diatta, G., et al. (2013). Plague epidemics and lice, Democratic Republic of the Congo. Emerging Infectious Diseases, 19(3), 505–506. http://doi.org/10.3201/eid1903.121329

Raoult, D. (2016). A Personal View of How Paleomicrobiology Aids Our Understanding of the Role of Lice in Plague Pandemics. Microbiology Spectrum, 4(4). http://doi.org/10.1128/microbiolspec.PoH-0001-2014

Drali, R., Mumcuoglu, K., & Raoult, D. (2016). Human Lice in Paleoentomology and Paleomicrobiology. Microbiology Spectrum, 4(4). http://doi.org/10.1128/microbiolspec.PoH-0005-2014

Tran, T.-N.-N., Forestier, C. L., Drancourt, M., Raoult, D., & Aboudharam, G. (2011). Brief communication: co-detection of Bartonella quintana and Yersinia pestis in an 11th-15th burial site in Bondy, France. American Journal of Physical Anthropology, 145(3), 489–494. http://doi.org/10.1002/ajpa.21510

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