Category Archives: public health

The Pathogen Buzz of 2016

by Michelle Ziegler

Altmetrics recently released the Top 100 scholarly articles list for the year (captured on 15 Nov 2016). Their ranking captures the public discussion on academic articles judged by shares of the online edition, news articles, blog posts and tweets that include the digital object identifier code (doi). (So if you want to improve the Altmetrics number of your papers make sure that all blog posts/tweets/news articles have the doi somewhere.) Note that generating discussion is not the same as being the best papers produced. At least one one this list, on ‘Patient 0’ HIV-1,  seemed to generate a fair amount of complaints.

Overall, the list was dominated by medical and health science (49) and biological science (14), altogether being 63% of the top 100 articles. Some of the other categories are a little vague, such as physical science (6) vs. earth and environmental science (6) vs. material science (1). History and archaeology combined to produce only six of the top 100 and one of them, on the ‘Tully monster’, really should be paleontology (or biology?). We also have to keep in mind that Altmetrics misses most of the humanities journals. The Altmetric scores in the top hundred have also approximately doubled between 2014 and 2016. The lowest score in 2016 is 1605 and the lowest score in 2014 was only 746.

One highlight this year is that 47% of the top 100 were either freely available or open access. I noticed about midway through this past year that papers expected to get a lot of attention were often freely available or open access. The difference between freely available vs open access may be whether or not the authors had to pay for the open availability (?). I wonder if the freely available remain free forever, or only until the news dies down?

Zika vector Aedes aegypti (Courtesy of CDC/Public Health Image Library #9261)

When it comes to pathogens, this year’s list comes with the distinctive buzz of a mosquito, Aedes aegypti, carrying this year’s emerging infectious disease, the Zika virus. Of the twelve papers directly related to infection, six are on Zika. Looking at the 2015 list, it’s clear that Zika put pathogens in the news this year. There are hardly no pathogen related papers in the 2015 list and in 2014, there were only five  – four on ebola and one on ancient Yersinia pestis. So clearly Zika has made a far bigger splash than even the much more lethal ebola.

Pathogens in the 2016 Top 100:

6. Rasmussen, S. A., Jamieson, D. J., Honein, M. A., & Petersen, L. R. (2016). Zika virus and birth defects—reviewing the evidence for causality. New England Journal of Medicine, 374(20), 1981-1987. DOI: 10.1056/nejmsr1604338

17. Zipperer, A., Konnerth, M. C., Laux, C., Berscheid, A., Janek, D., Weidenmaier, C., … & Willmann, M. (2016). Human commensals producing a novel antibiotic impair pathogen colonization. Nature, 535(7613), 511-516. DOI: 10.1001/jama.2016.0287

19. Singer, M., Deutschman, C. S., Seymour, C. W., Shankar-Hari, M., Annane, D., Bauer, M., … & Hotchkiss, R. S. (2016). The third international consensus definitions for sepsis and septic shock (sepsis-3). Jama, 315(8), 801-810.17. DOI: 10.1001/jama.2016.0287

20. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., … & Vizjak, A. (2016). Zika virus associated with microcephaly. New England Journal of Medicine, 374(10), 951-958. DOI: doi/10.1056/NEJMoa1600651

25. Miranda, R. C., & Schaffner, D. W. (2016). Longer contact times increase cross-contamination of Enterobacter aerogenes from surfaces to food. Applied and Environmental Microbiology, 82(21), 6490-6496. DOI:10.1128/aem.01838-1620.

31. McGann, P., Snesrud, E., Maybank, R., Corey, B., Ong, A. C., Clifford, R., … & Schaecher, K. E. (2016). Escherichia coli Harboring mcr-1 and blaCTX-M on a Novel IncF Plasmid: First report of mcr-1 in the USA. Antimicrobial agents and chemotherapy. DOI: 10.1128/aac.01103-16

37. Cao-Lormeau, V. M., Blake, A., Mons, S., Lastère, S., Roche, C., Vanhomwegen, J., … & Vial, A. L. (2016). Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. The Lancet, 387(10027), 1531-1539. DOI: 10.1016/s0140-6736(16)00562-6

46. Worobey, M., Watts, T. D., McKay, R. A., Suchard, M. A., Granade, T., Teuwen, D. E., … & Jaffe, H. W. (2016). 1970s and ‘Patient 0’HIV-1 genomes illuminate early HIV/AIDS history in North America. Nature, 539(7627), 98-101. DOI: 10.1038/nature19827

49. Fauci, A. S., & Morens, D. M. (2016). Zika virus in the Americas—yet another arbovirus threat. New England Journal of Medicine, 374(7), 601-604. DOI: 10.1056/nejmp1600297

54. Tang, H., Hammack, C., Ogden, S. C., Wen, Z., Qian, X., Li, Y., … & Christian, K. M. (2016). Zika virus infects human cortical neural progenitors and attenuates their growth. Cell stem cell, 18(5), 587-590. DOI: 10.1016/j.stem.2016.02.016

86. Liu, Y. Y., Wang, Y., Walsh, T. R., Yi, L. X., Zhang, R., Spencer, J., … & Yu, L. F. (2016). Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. The Lancet Infectious Diseases, 16(2), 161-168.54. DOI: 10.1016/S1473-3099(15)00424-7

92. Brasil, P., Pereira, Jr, J. P., Raja Gabaglia, C., Damasceno, L., Wakimoto, M., Ribeiro Nogueira, R. M., … & Calvet, G. A. (2016). Zika virus infection in pregnant women in Rio de Janeiro—preliminary report. New England Journal of Medicine. DOI: 10.1056/NEJMoa1602412

Before we leave the buzz of 2016, we have to mention this year also saw the passing of Dr. Donald Henderson (1928-2016) who led the effort to eradicate smallpox. Henderson died in August; his obituary from the New York Times can be found here.

Henderson administering a smallpox vaccine in about 1972 (WHO).

Landscapes of Disease Themed Issue

Untitled design.jpg

For the last couple years, I have been writing about a landscape-based approach to the study of infectious disease in general and historic epidemics in particular. When I first wrote about Lambin et al.’s now classic paper “Pathogenic landscapes” nearly three years ago, I did not know then that it would be so influential in my thinking or that the Medieval Congress sessions would be so successful. In the fall of 2014, Graham Fairclough and I began talking about ways that this first congress session could be represented in the journal he edits, Landscapes. This issue is a departure from their usual approach to landscape studies so I would like to thank Graham Fairclough for entrusting me with a whole issue. It has been a challenge for both of us, and I am proud of our product.

This issue represents the wide variety of studies that can be done all contributing to an understanding of past landscapes of disease. One of the reasons why I like the phrase landscape of disease, rather than simply landscape epidemiology, is that it opens up the array of disciplines that can be involved. In the study of diseases of the past, humanistic approaches can be as valuable as scientific methods. Both are required to build a reasonably coherent reconstruction of the past. Science and the humanities need to act as a check and balance on each other, hopefully in a supportive and collegial way.

The issue was published online a couple days ago. Accessing the journal through your library will register interest in the journal with both your library and the publisher, and would be appreciated. By now the authors should (or will soon) have their codes for their free e-copies if you do not have access otherwise.

Table of Contents

Landscapes of Disease by Michelle Ziegler. An introduction to the concept of ‘landscapes of disease’ and the articles in the issue. (Open access)

The Diseased Landscape: Medieval and Early Modern Plaguescapes by Lori Jones

The Influence of Regional Landscapes on Early Medieval Health (c. 400-1200 A.D.): Evidence from Irish Human Skeletal Remains by Mara Tesorieri

Malarial Landscapes in Late Antique Rome and the Tiber Valley by Michelle Ziegler

Epizootic Landscapes: Sheep Scab and Regional Environment in England in 1279-1280 by Philip Slavin

Plague, Demographic Upheaval and Civilisational Decline: Ibn Khaldūn and Muḥammed al-Shaqūrī on the Black Death in North Africa and Islamic Spain by Russell Hopley

plus seven book reviews. Enjoy!


Lambin, E. F., Tran, A., Vanwambeke, S. O., Linard, C., & Soti, V. (2010). Pathogenic landscapes: Interactions between land, people, disease vectors, and their animal hosts. International Journal of Health Geographics, 9(1), 54.

The Case for Louse-Transmitted Plague

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 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 sylvatic reservoir to distant human populations, is going to get a whole lot more complicated but also more interesting.


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.

Drancourt, M., Houhamdi, L., & Raoult, D. (2006). Yersinia pestis as a telluric, human ectoparasite-borne organism. The Lancet Infectious Diseases, 6(4), 234–241.

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.

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.

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.

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.

Little, L. K. (2011). Plague Historians in Lab Coats. Past & Present, 213(1), 267–290.

Malek, M. A., Bitam, I., & Drancourt, M. (2016). Plague in Arab Maghreb, 1940–2015: A Review. Frontiers in Public Health, 4, 18–6.

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.

Raoult, D. (2016). A Personal View of How Paleomicrobiology Aids Our Understanding of the Role of Lice in Plague Pandemics. Microbiology Spectrum, 4(4).

Drali, R., Mumcuoglu, K., & Raoult, D. (2016). Human Lice in Paleoentomology and Paleomicrobiology. Microbiology Spectrum, 4(4).

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.