Dogs as Plague Sentinels and Vectors

Marmot fighting a wild dog in northern Tibet (Source: China Tibet Online/ Xinhua)

I’ve been a little obsessed with thinking about dogs and the plague lately. Dogs are often overlooked in historic plague discussions because they usually survive plague and dog-specific fleas are not associated with transmitting plague. Yet, dogs can host many of the fleas common among rodents and others that do transmit the plague including the cat flea (Ctenocephalidis felis) and the human flea (Pulex irritans) (Gage, Montenieri, & Thomas 1994). In a case controlled study of nine US cases of bubonic and septicemic plague in 2006, having dogs in the home and particularly sleeping with a dog was a significant risk factor, probably by flea transfer (Gould et al, 2008).  There is also a growing awareness that dogs can also transmit pneumonic plague directly to humans. Like other aspects of plague biology, there is a lot going on under a veneer of normalcy.

Dogs do readily contract the plague; it’s just not apparent to casual observation. In the American state of New Mexico, 62 domestic dogs were diagnosed with plague just between the years 2003 and 2011 — 97% survived (Nichols et al, 2014).  The dogs were diagnosed by an increase of Yersinia pestis F1 antibody greater than four times greater than the recovered level, by isolation of Yersinia pestis from a body fluid or by direct flourescent antibody assay of a tissue specimen. All of them had some physical sign of infection with fever and lethargy being found in 100% of cases, but buboes or lymphadenopathy (enlarged lymph nodes) were found in only 23% and these were all in the jaw and neck region. The mean time for recovery was two days, although all but one did receive at least one dose of antibiotics. Potential sources of plague exposure are from prairie dogs, ground squirrels, chipmunks, and rabbits. Only three of the dogs had any fleas at all, but as these dogs were pets, most had received anti-flea treatment.

Monitoring plague in working dogs and other carnivores is the most efficient method of doing plague surveillance in the vast semi-arid grasslands that harbor some of the most enduring plague reservoirs. Dogs are especially useful because their immunity only lasts about six months, so a detectable level (titre) of plague antibody indicates recent contact with an infected animal. Gage, Montenieri, and Thomas (1994:6) estimated that  “sampling even a few rodent consuming carnivores, such as coyotes, can be roughly equivalent to sampling hundreds of rodents for evidence of plague infection”. The earliest serologic survey that I have found was done in Navajo lands in 1966-1968. In this same survey  in 1968, “the plague organism was isolated from a pool of fleas (Pulex irritans) taken from the household dogs of a person with plague” (Archibald & Kunitz 1971). Carnivores are now routinely monitored in the US.  Surveying herding dogs in Iran was able to show that the long unmonitored plague foci is still active (Esamaeili et al., 2013). Recent Chinese F1 antibody surveys in the Gansu province are more ominous: in 2012 4.55% of dogs were positive, but it had jumped to 10% of dogs by 2014 (Ge et al, 2014). Another  2014 survey of multiple Yersinia species in dogs found 25% of dogs in Gansu province and 18% of dogs in Qinghai province to be positive for Yersinia pestis F1 antibody, while no plague-free provinces had a single dog that had a positive antibody titre (Wang et al, 2014).

Consumption is the likely primary route of infection for dogs.  The 62 dogs from New Mexico are believed to have been primarily infected by consumption of a plague infected rodent or rabbit (Nichols et al, 2014). In a 2014 case study from China, an infected marmot was taken from a dog, butchered and divided among five dogs. All five dogs developed positive antibody titers for  plague and the shepherd who took the marmot from the dog developed pneumonic plague (but not his brother who butchered the marmot). Aerosol transmission was supported by  the isolation of Y. pestis from sputum and throat samples (Ge et al, 2014). One dog not fed the marmot was negative for the F1 antigen. Three of the 151 human contacts given prophylactic antibiotics developed an antibody titre but did not manifest disease. According to Chinese policy, the five positive dogs were euthanized and the local marmots were depopulated (Ge et al., 2014).

Dogs can transmit plague to humans through fleas that feed on the dog, fleas carried by the dog from the rodent source of the infection,  through bites or scratches, or by aerosols from dogs that develop a systemic infection. While dogs are usually thought of transmitting infected fleas to people, the  number of pneumonic cases linked to dogs is increasing. The first confirmed transmission of pneumonic plague from a dog to a person occurred in China in 2009 (Wang et al, 2015). The index case in turn transmitted pneumonic plague to eleven people. Three of these twelve cases died with the other nine cases confirmed by Y. pestis F1 antibody titres. All of the Y. pestis isolates were later typed to “biovar antiqua” — a reminder that older strains are still very virulent (Wang et al, 2009). In June 2104, in Colorado, a dog transmitted pneumonic plague to three caregivers, one of whom transmitted it to another person. All of four of these cases survived and 88 additional people were given prophylactic antibiotics (Runfola et al, 2015). Three of China’s 2014 plague cases in Gansu province within the Qinghai-Tibet plague focus area  were pneumonic plague in herders.  All three arrived at the medical center too late for effective antibiotic treatment and died (Li et al, 2016). Chinese authorities believe that two of these men may have contracted plague from infected dogs and the third directly from a marmot (Lie et al, 2016).

Dog transmitted plague seems to usually result in family or small settlement size outbreaks. I do wonder about the potential role of dogs in the Bronze Age cases of plague (Rasmussen et al, 2015). Dogs contracting plague by consumption of infected rodents and passing it on to human contacts seems possible with the tools of the Bronze Age strains. It might also be worth investigating the potential role of dogs in the beginning of the Great Manchurian Plague of 1910-1911, which focused on hunters who likely used dogs extensively. Indeed hunters in this region would feed sick marmots to their dogs believing that they could not contract the disease. Outbreaks of 100% lethal plague were not unknown among hunting families in Manchuria (Summers 2012: 122-124). Such a high mortality rate would suggest pneumonic plague.


Archibald, W. S., & Kunitz, S. J. (1971). Detection of plague by testing serums of dogs on the Navajo Reservation. HSMHA Health Reports.

Esamaeili, S., Azadmanesh, K., Naddaf, S. R., Rajerison, M., Carniel, E., & Mostafavi, E. (2013). Serologic Survey of Plague in Animals, Western Iran. Emerging Infectious Diseases, 19(9).

Gage, K. L., Montenieri, J. A., & Thomas, R. E. (1994). The role of predators in the ecology, epidemiology, and surveillance of plague in the United States, 20.Proceedings of the 16th Vertebrate. Pest Conference (W.S. Halverson& A.C. Crabb, Eds.) Published at Univ. of Calif., Davis. 1994.

Ge P, Xi J, Ding J, Jin F, Zhang H, Guo L, Zhang J, Li J, Gan Z, Wu B, Liang J, Wang X, Wang X, Primary Case of Pneumonic Plague in Marmata himalayana natural focus area Gansu Province, China, International Journal of Infectious Diseases (2014),

Gould, L. H., Pape, J., Ettestad, P., Griffith, K. S., & Mead, P. S. (2008). Dog-Associated Risk Factors for Human Plague. Zoonoses and Public Health, 55(0), 448–454.

Li, Y., Li, D, Shao, H., Li, H and Han, Y. (2016) Plague in China 2014 — All sporadic case report of pneumonic plague. BMC Infectious Disease. 16: 85.

Lin, Karen. (2014-07-02) Photo: Himalaya marmot eaten by wild dogs in N. Tibet. China Tibet Online.

Nichols, M. C., Ettestad, P. J., Vinhatton, E. S., Melman, S. D., Onischuk, L., Pierce, E. A., & Aragon, A. S. (2014). Yersinia pestis infection in dogs: 62 cases (2003-2011). Journal of the American Veterinary Medical Association, 244(10), 1176–1180. doi:10.2460/javma.244.10.1176

Rasmussen, S., Allentoft, M. E., Nielsen, K., Orlando, L., Sikora, M., Sjögren, K.-G., et al. (2015). Early Divergent Strains of Yersinia pestis in Eurasia 5,000 Years Ago. Cell, 163(3), 571–582. [Bronze Age cases]

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.

Salkeld, D. J., & Stapp, P. (2006). Seroprevalence Rates and Transmission of Plague (Yersinia pestis) in Mammalian Carnivores. Vector-Borne and Zoonotic Diseases, 6(3), 231–239.

Summers, William C. (2012) The Great Manchurian Plague of 1910-1911: The Geopolitics of an Epidemic Disease. Yale University Press.

Wang, H., Cui, Y., Wang, Z., Wang, X., Guo, Z., Yan, Y., et al. (2015). A Dog-Associated Primary Pneumonic Plague in Qinghai Province, China. Clinical Infectious Diseases, 52(2), 185–190. doi:10.1093/cid/ciq107

Wang, X., Liang, J., Xi, J., Yang, J., Wang, M., Tian, K., et al. (2014). Canis lupus familiaris involved in the transmission of pathogenic Yersinia spp. in China. Veterinary Microbiology, 172(1-2), 339–344. doi:10.1016/j.vetmic.2014.04.015

Plague News

You may have noticed that there have been several big plague papers in the last couple months.

I haven’t posted on them partly because I have been busy with other things, but partly also because I don’t attempt to keep up with the news cycle. Sometimes things need to incubate for a while. For my purposes, identifying a microbe in the context of a historical place and time has been more important than phylogeny. I do pay attention to phylogeny and it may sometimes provide insights I find useful, but I think its is far too early to attempt to write history based on phylogeny. We still can not predict likely transmission routes with any detail. It’s good to know there is evidence of persistence in Europe, so we can get rid of the odd notion that there have never been European plague foci.   I’ll be back in the next couple days with a new post on a different aspect of plague.

Environment, Society and the Black Death in Sweden

Environment, Society and the Black Death: An Interdisciplinary Approach to the Late Medieval Crisis in Sweden. Edited by Per Lagerås. Oxbow Books, 2016. 

9781785700545_1The Black Death is a bit of a phantom in this book. Like the human body casts of Pompeii, the Black Death is perceptible  by the void it left behind — a void in farm occupation, a void in building,  a void in the population/labor but ironically, also a void in mass burials. Without distinctive plague burials, this is how we should expect a scientific investigation of the plague and its  environment context to be. What these sometimes contradictory seeming voids mean is the challenge taken up in this book.  The studies presented in this book used pollen diagrams, dendrochronology, settlement archaeology and human remains to investigate the entire fourteenth century crisis with the clear signature of the Black Death apparent in each type of investigation.

When the Black Death reached Sweden in 1350, the kingdom was in pretty good shape compared to elsewhere in Northern Europe. Sweden seems to have avoided the Great Famine. The population was spread between small villages and isolated homesteads; there were no large urban areas on par with London or Paris. There was still room to expand settlement toward the uplands in the north-west. The relatively thin settlement and lack of large urban areas explains the lack of mass burials. Based on the population distribution and predicted mortality rate (comparable to the rest of northern Europe), they predict that the thin settlement allowed them to keep up with the burials along with some semblance of usual burial customs, such as coffins. The only indicator of plague deaths (or any epidemic) is the incidence of double and triple graves.  So it’s not a matter of discovering the Black Death burials, they have been in plain sight all along.

Staying with the bodies, their osteological sample included 4876 skeletons from 65 medieval churchyards, three execution sites, and two mass military graves spanning the entire medieval period in the region of Lund. Their primary measure of stress was projected height. The only finding of significance was that women were slightly taller (2.5 cm) in the generation after the Black Death. I think they could have made a little more of this considering that the nutrition of young women has a disproportionate effect on fertility, fetal and maternal health. Enough healthy women of reproductive age is a necessity for a population to recover from a mortality crisis. The overall stature of Swedes was on par with elsewhere in Europe and in the 14th century far shorter than modern Swedes. The average height for a man after the Black Death was only 172.5 cm,  (5′ 8″) and women at 162.7 (5’5″). They reached their low point in the 19th century only to sharply rebound to their tallest point in the 20th century.

The isotope data from selected skeletons from Lund, the largest urban district in Sweden, yielded a few surprises. They did find a diet change to include more animal and marine sources, but unlike elsewhere in Northern Europe, the switch occurred in the 12th century, not the 14th century. Could this explain why there is no evidence of the Great Famine in Sweden? Nearly two-thirds of the specimens from Lund had some marine sources in their diet. Zooarchaeological specimens suggest that cod was the primary marine source and that freshwater fish were not major contributors to the diet.  Regardless, there was no 14th century diet change that the isotopes could detect and no correlation between dietary changes and height. Strontium analysis does not indicate many non-natives after the initial establishment phase of Lund. The Black Death period (1350-1370) had the lowest number of non-locals of the medieval to early modern period. They suggest that this means that contact with the non-Swedish world was reduced during this period.

The bulk of this book addresses settlement and land use changes in the mid-fourteenth century. Beginning with dendrochronology, there is a hundred years gap from 1360 to 1460, reflecting the lack of need of new building or expansion after the Black Death. Amazingly, a few of the farm buildings dating to the pre-Black Death period are still standing. Farm abandonment and landscape change unfortunately can’t be as directly measured as dendrochronology.

The pollen data largely reflects the paradox pointed to in Sing Chew’s The Recurring Dark Ages: Ecological Stress, Climate Change and System Transformation (2006), that periods of human crisis allow ecological rejuvenation.  More simply what is bad for humans, is good for the environment. Periods of decreased human environmental exploitation (or resource extraction, if you prefer) allow the environment to recover.  Chew does not address the fourteenth century, which we might call a Dark Age near miss, a time when the Old World tottered on the brink of another possible Dark Age, but the similarities still make a useful comparison (and open up some interesting questions).

In the decades after 1350, the pollen suggests that arable fields decreased, conversion to pasture and increased woodland expansion. The conversion of unused fields to pasture or hay kept those fields from regenerating their woodlands and making it easier to bring them back into arable production. Yet, there was still considerable woodland regeneration.  They note that seedlings that sprouted in the years after the Black Death formed a mature forest that lasted in some areas for 300+ years. A mature forest with 300+ year old trees will seem like a virgin forest, but it is not; it is still an anthropomorphic landscape.

“In summary the late-medieval crisis and in particular the population drop initiated by the Black Death in 1350 did not only result in profound and long-term social changes, but also in environmental and ecological changes. These changes were not only passive consequences of the crisis – they also affected the course of the crisis through different feedback mechanisms, both positive and negative.”(Lagerås, 2016, loc 3603)

They also note that the only previous rejuvenation of woodlands in Europe occurred in the sixth century around the time of the first plague pandemic. I’m encouraged to see their interest in comparing the 14th century environmental context/consequences to the sixth century. It is refreshing to read a book written with such a clear, scientific tone and approach.

They note that the expansion of woodland allowed a rejuvenation of biodiversity mentioned in  a 1376 royal letter that claimed more wolves and bears were damaging humans and livestock. While the abandonment would have decreased hunting pressure, it is also likely that the expansion of the woodland allowed a flourishing of the entire tropic cascade that was capped by predators like wolves and bears. We are more accustomed to thinking of tropic cascades as being suppressed by top down predation (often caused by humans), but the cascade can also bloom bottom up.  While on the topic of biodiversity,  a discussion of small mammals that could play a role in plague transmission during the 1350 epidemic and later epidemics would have been helpful. This ecological flourishing will radically change the landscape and human relationship to it. What effect, if any, did this have on later plague transmission? In this regard, their comparisons to an 18th century plague would have been just about when the post-Black Death ecological changes were giving way to expansion of arable farmland again and the population had rebounded.

The complexity of the ecological and settlement data is a measure of the long-term contextual changes caused by a single massive epidemic and its aftershocks. Populations would have been moving within the country for many years as heirs took possession of better land, and families depleted of heirs dwindled away over time. They note that the post-Black Death period brings about the end of the self-sufficient manor system. Social order evolves into a more specialized and interdependent system. The ecological changes slowly rolled out as fields turned into pastures or were left fallow; forest encroachment and development occurred over many years. This book is a work in progress on the environmental history of Sweden’s anthropomorphic landscape and its people. It should be considered in the context of other environmental studies of the fourteenth century crisis from Scandinavia, Britain and Ireland, Iceland, and the Northern European continent. I look forward to seeing how their work develops in the future.