Body lice, Yersinia pestis Orientalis, and Black Death.
Article Type: Report
Subject: Lice (Research)
Yersinia pestis (Research)
Plague (Causes of)
Plague (Research)
Authors: Welford, Mark
Bossak, Brian
McLean, Robert G.
Fall, Michael W.
Pub Date: 10/01/2010
Publication: Name: Emerging Infectious Diseases Publisher: U.S. National Center for Infectious Diseases Audience: Academic; Professional Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2010 U.S. National Center for Infectious Diseases ISSN: 1080-6040
Issue: Date: Oct, 2010 Source Volume: 16 Source Issue: 10
Topic: Event Code: 310 Science & research
Accession Number: 238895963
Full Text: To the Editor: A scientific debate with public health implications wages: What caused the medieval European plague epidemics known as Black Death? Recent articles note inconsistencies between a rat fleaborne pandemic of Yersinia pestis (the bacterium that causes bubonic plague) and the documented characteristics of Black Death (1, among others). Ayyadurai et al. (2) acknowledge that a rat flea-only hypothesis does not fit Black Death observations, but they resolve theoretical transmission inconsistencies through a louse-borne hypothesis. Ayyadurai et al. base their surety of fact--that medieval "plagues" were caused by Y. pestis infection--on a 2007 study (3) in which 5 of 36 teeth of "plague" victims, none of which were dated to the Black Death era (1347-1351), contained biological evidence of Y. pestis. The 3 locations in that study were all port cities: 2 on the Mediterranean Sea and 1 on the Rhone River. As Duncan and Scott (4) note, bubonic plague most likely existed endemically near ship-borne trade, unlike the fast-moving epidemic fronts exhibited by medieval "plagues." Moreover, Gilbert et al. (5) found no Y. pestis DNA in 61 skeletons from primarily nonport locations in England, France, and Denmark.

We do not dispute the authors' claim that Y. pestis might have been present in some skeletons from port cities in France, or that body lice might, under certain circumstances, transmit the Orientalis biotype of Y. pestis; their work appears careful and considered. However, given the differences mentioned above and improved knowledge on the rapidity of virus mutation and worldwide transmission potential, we merely argue that the simplest explanation for medieval plagues has yet to be ruled out: that they may have resulted from a human-to-human transmitted virus. Adding complexity to an already complicated etiologic theory, and stating such as historical fact based on limited geography and sample size, does not seem congruent with Occam's razor.

Mark Welford and Brian Bossak

Author affiliation: Georgia Southern University, Statesboro, Georgia, USA

DOI: 10.3201/eid1610.100683

References

(1.) Welford MR, Bossak BH. Validation of inverse seasonal peak mortality in medieval plagues, including the Black Death, in comparison to modern Yersinia pestis-variant diseases. PLoS ONE. 2009;4:e8401. DOI: 10.1371/journal.pone.0008401

(2.) Ayyadurai S, Sebbane F, Raoult D, Drancourt M. Body lice, Yersinia pestis Orientalis, and Black Death. Emerg Infect Dis. 2010;16:892-3.

(3.) Drancourt M, Signoli M, Vu Dang L, Bizot B, Roux V, Tzortzis S, et al. Yersinia pestis Orientalis in remains of ancient plague patients. Emerg Infect Dis. 2007;13:332-3. DOI: 10.3201/eid1302.060197

(4.) Duncan CJ, Scott S. What caused the Black Death? Postgrad Med J. 2005;81:315-20.

(5.) Gilbert MT, Cuccui J, White W, Lynnerup N, Titball RW, Cooper A, et al. Absence of Yersinia pestis-specific DNA in human teeth from five European excavations of putative plague victims. Microbiology. 2004;150:341-54.

Address for correspondence: Mark Welford, Georgia Southern University, Geology and Geography, 68 Georgia Ave, Bldg 201, Statesboro, GA 30460-8149, USA; email: mwelford@georgiasouthern.edu

To the Editor: The letter of Ayyadurai et al. (1) reminded us of a little-known paper (2) on rats and Black Death by our colleague and mentor David E. Davis. He researched and wrote in his retirement after years of research and reflection on rat ecology and rodent-borne diseases (3,4). Rattus rattus is commonly recognized as the vertebrate host of flea-borne plague that swept through Europe in the 1300s, killing >50% of the population. Davis believed this explanation did not fit what he knew of the ecologic requirements of fleas and black rats. He studied reports of archeologic excavations and reviewed poems, medieval bestiaries, and paintings and concluded that these rats were scarce during the Black Death era.

His theory, based on historical information and investigative trips to Europe, was that invasive rats, if present, mostly occurred in low densities in port areas, not in rural inland areas. He noted that the expected rodent die-offs with bubonic plague were not associated with human epidemics and that rodent fleas would not have been active during winter to transmit plague. Flea-borne transmission from rodents usually causes a few deaths per household, but deaths of entire households commonly occurred in the medieval epidemics. Human-to-human transmission of pneumonic plague must have occurred, but as described by Ayyadurai et al., there was evidence of human bubonic plague, suggesting vector involvement. Davis did not present a viable reservoir/vector hypothesis for plague transmission; this and the later, well-known association of R. rattus and other rodents with plague throughout the world, may partially explain why his ideas received little attention. The finding that human body lice can be bubonic plague vectors suggests a mechanism for human-to-human transmission continuing during winter in inland areas and, as suggested by the authors, could also explain total deaths in households.

Robert G. McLean and Michael W. Fall

Author affiliation: National Wildlife Research Center, Fort Collins, Colorado, USA

Address for correspondence: Robert G. McLean, National Wildlife Research Center, US Department of Agriculture/Animal and Plant Health Inspection Service/Wildlife Services, 4101 LaPorte Ave, Fort Collins, CO 80521, USA; email: r.mclean38@yahoo.com

DOI: 10.3201/eid1610.100822

References

(1.) Ayyadurai S, Sebbane F, Raoult D, Drancourt M. Body lice, Yersinia pestis, and Black Death. Emerg Infect Dis. 2010;16:892-3.

(2.) Davis DE. The scarcity of rats and the Black Death: an ecological history. J In terdiscip Hist. 1986;16:455-70. DOI: 10.2307/204499

3. Anonymous. Profiles of previous Wildlife Disease Association leaders: David E. Davis 1913-1994. J Wildl Dis 1995; 31(1 suppl):15.

4. Davis DE. The characteristics of rat populations. Q Rev Biol. 1953;28:373-401. DOI: 10.1086/399860

In Response: Commenting on our recent demonstration that the human body louse was a likely vector of Black Death (the medieval European plague epidemics) (1), Welford and Bossak (2) point out that quantitative and qualitative inconsistencies in data for Black Death and modern plague argue against concluding that Yersinia pestis is the etiologic agent of Black Death (3). These authors acknowledge the paleomicrobiologic demonstration of Y. pestis in human remains collected at ports, yet they argue that such demonstration remains to be performed for human remains collected from inland burial sites (2).

Careful review of the literature indicates that 3 unrelated scientific teams have now demonstrated the presence of Y. pestis-specific biomolecules in 14th-18th-century human remains in 11 sites in Europe. These locations include 7 nonport, inland sites <650 km from the coasts (4-6) in addition to 3 Justinian (nonport) locations (4,7). Therefore, the fact that Y. pestis was the etiologic agent of Black Death can no longer be disputed; the inconsistencies correctly noted by Welford and Bossak actually question the reservoir and the vector of Y. pestis during the Black Death and the following epidemics rather than its cause. McLean and Fall remind us that the cumulative work of their mentor, David E. Davis, suggested that black rat ectoparasites could not have been likely vectors of medieval plague in Europe, based on the facts that expected die-offs of rats were not reported and that the rodents' fleas would not have been active during winter in medieval Europe (8).

McLean and Fall acknowledge that our experimental data pave the way toward an alternative scenario of body louse-borne transmission of the Black Death. Such transmission of Y. pestis was observed by Blanc and Baltazard during a cluster of bubonic plague cases in households in Morocco during World War II (9). These authors demonstrated that the body louse could be infected when living on a septicemic patient, could stay alive for 7 days with infectious feces, and could transmit plague (9). Demonstration of Y. pestis in human lice collected from Black Death burials would be a step toward understanding the epidemiology of Black Death; this technically demanding approach has been successfully used to assess the transmission of typhus in soldiers of Napoleon's Grand Army buried in Vilnius, Lithuania (10).

In agreement with these observations and those reported by Welford and Bossak (3), our work clearly indicates that Y. pestis could be efficiently transmitted by the human louse (1), a potential vector of Black Death because of its high prevalence in medieval Europe (11). Far from "adding complexity to an already complicated etiology theory," as Welford and Bossak stated, it seems to us that the cumulative evidence provided by paleomicrobiologic demonstration and by our recent work (1) clarifies the epidemiology of the Black Death and the subsequent epidemics. Louse transmission of Y. pestis also explains inconsistencies rightly noted by Welford and Bossak and provides a reason for the current plague cases in poor areas of the world where poor hygiene is common. A search for alternative hypotheses, including the previous viral hypothesis for Black Death, may not be necessary (2).

The analogic reasoning based on observations of current infectious diseases cannot be applied to the medieval Black Death. Paleomicrobiologic evidence and historical data force us to change the paradigm and to question the established dogma about the epidemiology of plague. McLean and Fall remind us that, even in science, alternative hypotheses have trouble challenging dogma (8). Black Death is one of many areas at the intersection of microbiology and history for which many hypotheses have been proposed and none has received confirmation; these hypotheses have been repeated for so long that they became accepted as demonstrated truths.

Michel Drancourt and Didier Raoult

Author affiliations: Universite de la Mediterranee, Marseille, France; and Editorial Board, Emerging Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA

DOI: 10.3201/eid1610.100946

References

(1.) Ayyadurai S, Sebbane F, Raoult D, Drancourt M. Body lice, Yersinia pestis Orientalis, and Black Death. Emerg Infect Dis. 2010;16:892-3.

(2.) Welford M, Bossak B. Body lice, Yersinia pestis Orientalis, and Black Death [letter]. Emerg Infect Dis. 2010;16:1651.

(3.) Welford MR, Bossak BH. Validation of inverse seasonal peak mortality in medieval plagues, including the Black Death, in comparison to modern Yersinia pestis variant diseases. PLoS One. 2009;4:e8401. DOI: 10.1371/journal.pone.0008401

(4.) Drancourt M, Roux V, Dang LV, TranHung L, Castex D, Chenal-Francisque V, et al. Genotyping, Orientalis-like Yersinia pestis, and plague pandemics. Emerg Infect Dis. 2004;10:1585-92.

(5.) Pusch CM, Rahalison L, Blin N, Nicholson GJ, Czarnetzki A. Yersinial F1 antigen and the cause of Black Death. Lancet Infect Dis. 2004;4:484-5. DOI: 10.1016/ S1473-3099(04)01099-0

(6.) Bianucci R, Rahalison L, Massa ER, Peluso A, Ferroglio E, Signoli M. 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). Am J Phys Anthropol. 2008;136:361-7. DOI: 10.1002/ajpa.20818

(7.) Wiechmann I, Grupe G. Detection of Yersinia pestis DNA in two early medieval skeletal finds from Aschheim (Upper Bavaria, 6th century AD). Am J Phys Anthropol. 2005;126:48-55. DOI: 10.1002/ ajpa.10276

(8.) McLean RG, Fall MW. Body lice, Yersinia pestis Orientalis, and Black Death [letter]. Emerg Infect Dis. 2010;16:1651-2.

(9.) Blanc G, Baltazard M. Recherches experimentales sur la peste. L'infection du pou de l'homme: Pediculus corporis de Geer. CR Acad Sci. 1941;213:849-51.

(10.) Raoult D, Dutour O, Houhamdi L, Jankauskas R, Fournier PE, Ardagna Y, et al. Evidence for louse-transmitted diseases in soldiers of Napoleon's Grand Army in Vilnius. J Infect Dis. 2006;193:112-20. DOI: 10.1086/498534

(11.) Raoult D, Roux V. The body louse as a vector of reemerging human diseases. Clin Infect Dis. 1999;29:888-911. DOI: 10.1086/520454

Address for correspondence: Michel Drancourt, Unite des Recherche sur les Maladies Infectieuses et Tropicales Emergent, CNRS UMR 6236, Faculte de Medecine, 27 Blvd Jean Moulin, 13385 Marseille CEDEX 5, France; email: michel.drancourt@univmed.fr
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