Dogs as Plague Sentinels and Vectors

W020140703377708061490_r75
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.

References:

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). http://doi.org/10.3201/eid1909.121829

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), http://dx.doi.org/10.1016/j.ijid.2014.12.044

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. http://doi.org/10.1111/j.1863-2378.2008.01132.x

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. http://www.vtibet.com/en/news_1746/focus/201407/t20140703_209395.html

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. http://doi.org/10.1016/j.cell.2015.10.009 [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. http://doi.org/10.1089/vbz.2006.6.231

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