The old paradigm is dead! Long live the new paradigm!
Rebecca Eisen, David Dennis, and Kenneth Gage just published an article gathering all the evidence that should put an end to the blocked flea model as the only significant method of plague transmission. They summarize the data proving that unblocked fleas can and do transmit Yersinia pestis at levels that readily cause infection in rodents and humans. They call all transmission by unblocked fleas early-phase transmission (EPT), even in flea species that never block.
Important findings summarized:
- The blocked flea model – that only a biofilm blocked Xenopsylla cheopis which cannot eat so it tries to aggressively feed and regurgitates high numbers of Yersinia pestis into the bite site – is insufficient to account for either epizootics or large human outbreaks. Blocked fleas do transmit the plague but are simply insufficient to account for the speed and volume of epizootic and epidemic transmission.
- Transmission can occur as quickly as the very next blood meal taken by the flea, at times within 1-2 hours. Y. pestis does not need to replicate in the flea for transmission to occur. This makes it much more likely that the flea will survive long enough to transmit the infection.
- Early phase transmission has been experimentally observed to cause infections after exposure to a single Oropsylla montana flea. Therefore, exposure to large numbers of unblocked infected fleas is not required for transmission. Epidemiologic findings suggest that most US cases come from bites from a single or at most a few fleas, and this is consistent with findings around the world where fleas that do not block are primary vectors.
- Many reservoirs of plague are maintained by fleas that never block. Prairie dog reservoirs in the western US and great gerbil reservoirs in central Asia are both maintained by fleas that are never blocked by a biofilm.
“In short, EPT was observed in all flea species evaluated at varying temperatures. Transmission occasionally occurred as early as 3 h post-infection but usually was observed over 1-4 dpi [days post infection]. Although all flea species tested were capable of EPT, efficiency in these studies varied among species, suggesting that some fleas are likely to be more important than others in the rapid spread of plague in nature, especially those that are both efficient transmitters and abundant on susceptible hosts.” (p. 3)
- Strains of Y. pestis that can not form a biofilm transmit as effectively by EPT as biofilm competent strains. Virulence factors that are necessary for biofilm production are not necessary for EPT.
- EPT – compared to a contaminated “dirty needle” – is a mechanical form of transmission that “requires no modification or multiplication of the pathogen in the vector for transmission to occur” (p. 4).
- In the pre-antibiotic era, many human bubonic plague infections and all septicemic and pneumonic cases would have produced bacteremia levels sufficient to infect fleas for EPT. In the 71 fatal plague cases recorded by the CDC between 1956 and 2013, 86.8% were either primary or secondary septicemic cases.
“Epidemic support in favor of interhuman flea borne transmission comes from records of limited bubonic plague outbreaks in isolated rural communities under exceptional circumstances of heavy human flea infestations, high familial attack rates, and a lack of evidence for concurrent rat-flea borne plague. … [studies in Africa, the Middle East and the Andes mentioned]… Based on epidemiologic pattern of person to person spread, especially the high attack rates among contacts of the sick, an absence of domestic rats, and an unusual abundance of P. irritans infesting villages and their homes, investigators concluded that the outbreak resulted from infective bites by P. irritans.” (p. 7-8)
- They note that interhuman plague transmission by Pulex irritans has been documented early in the 20th century and supported by laboratory experiments. As covered here a year ago, infected Pulex irritans were recovered from the homes of plague patients in Madagascar in 2013. They end with a call for more work on P. irritans to evaluate its role in modern and historical human epidemics.
It is worth noting here that throughout the article they cite many studies using many different fleas. EPT studies have also been demonstrated for mouse fleas (Aetheca wagneri Baker) and cat fleas (Ctenocephalides felis). I’ve never really understood why studies of historic plagues often overlook mice as a source of fleas.
I also have to add that mechanical transmission by the flea makes a lot of evolutionary sense. It gives evolution a place to start tinkering. ‘Good enough’ is the stuff of evolution! Optimization only occurs after a very long evolutionary process, and may never be achieved. The fact that X. choepis evolved a method (via bioflim blockage and regurgitation [LPT]) to keep transmission going longer does suggest that the rat flea has been historically important to Y. pestis evolution. Obviously, mechanical transmission has also allowed Y. pestis to expand into areas and exploit new opportunities where a more complicated, required transmission system would have been an obstacle.
Experiments proving that EPT is possible are scattered over the last 50 years! And, yet the old paradigm still reigned. Why? Obviously, there has been a lack of communication within science and between science and the humanities. It would really be helpful for a historian of 20th-century science to look into how this could have happened.
Eisen, R. J., Dennis, D. T., & Gage, K. L. (2015). The Role of Early-Phase Transmission in the Spread of Yersinia pestis. Journal of Medical Entomology, tjv128–10. http://doi.org/10.1093/jme/tjv128. Advanced access, Aug. 19, 2015. (Open access)