The Black Death, which killed millions throughout Europe in a pandemic stretching from the 14th to 19th centuries, was likely spread by parasites such as fleas and lice carried on the human body.

While rats have long been blamed for spreading the fatal disease throughout Europe, researchers at the University of Oslo in Norway and the University of Ferrara in Italy now believe humans and their parasites were the biggest carriers.

"There are so many questions that this pandemic raises and how it spread so quickly is one of them," said Katharine R. Dean, lead author on a paper published Monday in the journal Proceedings in the National Academy of Sciences.

Dean and her colleagues studied nine outbreaks of the plague from 1348 to 1813 in European cities, including Barcelona, Florence, London, Stockholm, Moscow and Gdansk, Poland. A total of 125,000 people died in those outbreaks, sometimes so quickly that they could not be buried properly.

The bacteria killing them was Yersinia pestis, called bubonic plague or the Black Death, and it resulted in three significant plague periods in Europe.

Second Pandemic outbreaks

The period of the 14th to the 19th centuries, the time of the Second Pandemic, was the focus because there are fairly reliable official records of death rates as well as contemporary descriptions of the disease, Dean said.

An archaeologist works on March 10, 2015, at the site where eight mass graves with more than 200 skeletons were found under the Monoprix Reaumur Sebastopol store in Paris. Experts believe they are victims of an outbreak of bubonic plague in the Middle Ages. (Philippe Wojazer/Reuters)

The First or Justinian Pandemic in 541-544 was too early to result in accurate records.

Nor are rats blameless — they are believed to be carriers of the disease in the Third Pandemic, starting in 1855, Dean said. But that plague was accompanied by "rat falls," or mass deaths of rattus rattus in the streets.

The rapid spread of Yersinia pestis in the Second Pandemic is considered mysterious, said Dean, who is a PhD researcher interested in infectious disease epidemiology.

Dean studied the spread of plague using what is known about its transmission rates and the life cycles of human fleas and lice.

Working with researchers from Norway and Italy, she created mathematical models of contagion, comparing a human ectoparasite model (human fleas and lice) with transmission by rats and fleas and human-to-human transmission (via droplets in the air).

Plague still with us

The human fleas and lice model most closely coincides with the mortality rates in seven of the nine European cities. Florence, in the year 1400, lost 10,215 people, London in 1563-64 lost 16,886 and Moscow in 1771 saw 53,642 deaths.

"Plague is undeniably a disease of significant scientific, historic and public interest and is still present in many parts of the world today. It is therefore crucial that we understand the full spectrum of capabilities that this versatile, pandemic disease has exhibited in the past," the researchers concluded in their paper.

In a 1941 outbreak of plague in Morocco, plague-infected body lice are known to have played a role. Human parasites were observed in recent outbreaks of plague in Congo, Tanzania and Madagascar, although their role has not been studied.

"We're lucky today because there are not a lot of parasites because of higher standards of hygiene. That has helped to keep it down," Dean said.

Dean is fascinated with questions of how disease spread during Europe's great pandemics. The question of why it re-emerged several times over a 450-year period remains.

Lessons from the plague genome

Other researchers also are interested in what the Black Death can tell us about pandemics and controlling disease when antibiotics may not be effective.

In 2011, an international team — led by researchers at McMaster University and the University of Tubingen in Germany —- sequenced the entire genome of Yersinia pestis.

In 2016, that research led to confirmation that it was the same bacteria that caused the Black Death or Second Pandemic.

Hendrik Poinar, director of the McMaster Ancient DNA Centre, said researchers are now studying the genetics of various strains of the disease from China across Asia and into Europe.

"We want to know how it moved across the world," he said, but a bigger question is why it was so virulent.

The 1918 Spanish flu is thought of as a huge pandemic, but its virulence was a "drop in the bucket" compared to the Black Death, which had a much higher mortality rate, Poinar said.

"Losing so many people at once had a huge cultural impact," he said. "People are fascinated with it from the cultural perspective."