Underestimated parasites: Body lice may have been the main vectors of the great plague epidemics of the Middle Ages. Because these blood-sucking insects are surprisingly good carriers of the plague pathogen – even better than fleas, as a study reveals. The plague bacterium Yersinia pestis not only accumulates in the lice’s intestines, but also infects the secretory glands that lubricate their proboscis. The lice release a corresponding number of pathogens during their blood meal.
Whether in the Stone Age, antiquity or the “Black Death” in the Middle Ages: the plague has repeatedly caused fatal epidemics – in the Middle Ages a third of the European population even died from it. The plague pathogen, the bacterium Yersinia pestis, originally came from Asia and was introduced to Europe several times via maritime trade and the Silk Road. Once there, rats and their fleas became the main carriers of the disease – or so it was previously thought.
However, a study in 2018 raised doubts about this scenario. Models of the spread of plague in past outbreaks suggested that rats played only a minor role, at least in the “Black Death” of the Middle Ages. Instead, it is believed that the plague pathogen was usually transmitted directly through blood-sucking human fleas and lice.
Body louse as an epidemic helper?
David Bland and his colleagues from the US National Institute of Allergy and Infectious Diseases (NIAID) in Montana may have found the real culprit in the spread of the “Black Death”: the body louse (Pediculus humanus humanus). “This louse is an obligate bloodsucker with humans as its only host,” explains the team. The louse pierces the skin five to six times a day and sucks blood. Although body louse infestations are rare today due to better hygiene, “lice infestation” used to be a daily occurrence.
But despite its widespread distribution, especially in the Middle Ages, the body louse was previously considered a poor carrier of the plague. Studies have provided contradictory results as to how many pathogens she transmits while sucking blood and whether she dies of the plague beforehand. That’s why Bland and his team have now examined this in more detail.
Two ways to the next victim
For their study, the researchers marked plague bacteria with a fluorescent dye and mixed them with human blood. Body lice then sucked this blood through a skin-like membrane. Then the infected lice were divided into two groups: “We decided to compare two scenarios through which people come into contact with infected lice during a plague outbreak,” explain Bland and his colleagues.
In the first scenario, the body louse changes its host immediately after sucking blood on the plague patient – for example through direct physical contact between the two people. Around three hours after their own infection, the next blood meal takes place on a victim who is not yet infected – in the experiment this was a new, plague bacteria-free blood container. In the second scenario, the louse remains hidden in clothing, bedding and other hiding places for a long time before it can find a new host after a fasting period of around 18 hours.
Successful infection
The evaluations revealed that although 33 to 46 percent of the body lice died after being infected with the plague, the rest survived and developed a chronic infection. “40 to 60 percent of these lice in both groups remained infected a week later,” report Bland and his team. While sucking blood, these lice transferred medium to high doses of the plague bacteria to the blood reservoirs of the simulated hosts.
“Around 20 hours after their infection, the lice had transmitted the pathogen to 100 percent of the reservoirs,” the researchers said. The group of lice with the forced break was even more efficient: They transmitted more plague pathogens to the simulated next host than their conspecifics with the immediate host change. However, the amount of bacteria in both groups was more than sufficient to cause a plague infection, as the scientists explain.
Are lice rather than fleas the main culprit?
“Our results suggest that body lice are better vectors of plague bacteria than previously thought,” say Bland and his colleagues. “This supports the hypothesis that these lice were involved as vectors in previous plague outbreaks.” In addition, the body lice lack some crucial immune genes to fight off infection with gram-negative bacteria such as Yersinia pestis, the team says. As a result, they become infected easily and promote the proliferation of the pathogen in their bodies.
“The human flea Pulex irritans was widespread in households during the medieval plague epidemic,” explain the researchers. “But we examined the vector competence of the human flea again in more detail – and classified it as a rather poor transmitter of the plague bacteria.” Contrary to previously assumed, the plague bacteria do not clog the flea’s forestomach, which would encourage it to suck blood excessively.
Head gland as a “nest” of plague bacteria
The fluorescence analysis of the lice provided another surprise: Although the plague bacteria accumulated in many animals primarily in the digestive tract, some also showed bacterial accumulation in the head area. “This was unexpected, because we had not previously known of any microbial infections that attack structures in the lice’s head,” wrote Bland and his team. Interestingly, the lice with this head infection even transmitted more plague pathogens than their conspecifics.
But why? Further analysis revealed that the plague bacteria collected in these infected lice in the so-called Pavlovsky glands. “These glands are connected via thin ducts to the chamber in which the animals’ retractable proboscis sits,” explain the researchers. The secretion of the glands probably serves as a lubricant, facilitating the movement of the proboscis during the blood meal. However, in the case of lice infected with plague, this means that the bacteria are transmitted even more efficiently into the host.
“We have discovered that body lice not only transmit the plague better than previously thought – they also do so in more than one way,” the researchers state. The plague bacteria reach and enter their human host via the secretion of the Pavlovsky glands as well as the saliva and feces of the lice. (PLoS Biology, 2024; doi: 10.1371/journal.pbio.3002625)
Source: PLOS
May 22, 2024 – Nadja Podbregar