The Cloaca Maxima (The Giant Sewer), which burrows beneath the Roman Forum and the site of an ancient livestock market before emptying into the Tiber River, predates the Roman Empire.
The mile-long tunnel is believed to have been constructed in the fifth century before Christ under the orders of Tarquin the Proud, the last king of Rome before it became a republic.
The impressive structure was subsequently mentioned by Livy.
But decades of inadequate maintenance mean that it is clogged with debris and silt, raising fears of blockages and collapses.
An ambitious operation to clean and maintain the ancient drain got under way on Wednesday and is expected to take two years.
"We will free the drain of detritus and sediment that is impeding the flow of water," Elisabetta Bianchi, a cultural heritage official, told La Repubblica newspaper.
"We still need to get funding so we will proceed bit by bit, but the hope is to complete the work within two years." Cracks and fissures in the tunnel were studied and mapped last year, after Rome was hit by severe autumn flooding.
At one point the Tiber was so swollen that the point at which the Cloaca Maxima meets the river was almost concealed by raging flood waters.
The flooding had shown up the "inadequacies" of the centuries-old drain, said Maria Grazia Filetici, an architect with Rome's cultural heritage authority.
"What was conceived as a great project to make Rome safer (from flooding) by King Tarquin has instead become a danger for modern-day Rome," she said.
Engineers will have to shift huge quantities of rubbish clogging up the tunnel, including plastic bags, tangled electric cables and other detritus, said officials.
The Cloaca Maxima was originally dug as a canal by the early inhabitants of Rome, but was subsequently covered over to become a subterranean sewer.
It was maintained throughout the Roman Empire and into the medieval era and was ultimately incorporated into the city's modern sewerage system.
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