In late January, as the new coronavirus was beginning to spread from China’s Hubei province, a group of lay Buddhists traveled by bus to a temple ceremony in the city of Ningbo — hundreds of miles from Wuhan, center of the epidemic.
It was a sunny day with a gentle breeze, and the morning service was held al fresco, followed by a brief luncheon indoors.
A passenger on one of the buses had recently dined with friends from Hubei. She apparently did not know she carried the coronavirus. Within days, 24 fellow passengers on her bus were also found to be infected.
It did not matter how far a passenger sat from the infected individual on the bus, according to a study published in JAMA Internal Medicine on Tuesday. Even passengers in the very last row of the bus, seven rows behind the infected woman, caught the virus.
The only factor that may have mitigated the risk of infection was sitting near a window that could be opened, or near the door.
The incident adds to a large body of evidence indicating that the coronavirus can be transmitted by tiny particles that linger in the air, and not just through large respiratory droplets that fall quickly to the ground.
The World Health Organization acknowledged that the virus may be airborne in July and that these particles may seed superspreader events in closed spaces like restaurants and workplaces.
The new study “adds strong epidemiological evidence that the virus is transmitted through the air, because if it were not, we would only see cases close to the index patient — but we see it spread throughout the bus,” said Linsey Marr, a professor of civil and environmental engineering at Virginia Tech and a leading expert on airborne viruses.
The two buses carrying passengers to the event had cooling units that were recirculating air inside the vehicles.
“That would facilitate the virus in the air and spread it around the bus,” Marr said.
None of the 60 passengers on the second bus was infected.
Dr. Muge Cevik, an expert on infectious diseases and virology at the University of St. Andrews School of Medicine in Scotland, said that the outbreak was likely caused by a combination of factors: a long trip, a confined environment, a crowded bus and an individual who was probably extremely contagious because she was in the early stages of the infection.
“There isn’t really a dichotomy between aerosol and droplet transmission,” Cevik said. “There have to be multiple things happening at the same time for this type of high risk transmission to occur. This was the wrong place, the wrong time, the wrong person.”
The study’s authors, who are physicians with the Chinese Center for Disease Control and Prevention, concluded that “future efforts at prevention and control should consider the potential for airborne spread of COVID-19.” The study was published previously online as a preprint.
The outing to the Buddhist temple was what scientists refer to as a natural experiment. It took place Jan. 19, when there were still no confirmed COVID-19 cases reported in Ningbo. The circumstances conveniently allowed for a comparison between similar passengers on two different buses.
Some 300 people attended the temple ceremony, but only 128 made the 50-minute trip by bus. One bus carried 68 passengers, including the individual who was infected, while the second bus carried 60 people. None of the worshippers wore masks.
The paper in JAMA Internal Medicine does not describe the infected individual and says the person did not have symptoms until the after returning from the temple. But a version of the study published in China says the individual was a 64-year-old woman and that she developed symptoms Jan. 18, a day after dining with guests from Hubei and a day before going to the temple. She took medicine but did not see a doctor.
“The Chinese paper says the index case was unwell the day before going to the temple, so she was probably very infectious, because we know that viral load is really high around the time of symptom onset,” Cevik said.
The outdoor ceremony lasted 2 1/2 hours and was followed by a brief lunch, which took place in a spacious room that did not have recirculating air-conditioning. When the passengers returned to their buses, they took the same seats they had occupied earlier.
In addition to the passengers who became infected, another seven individuals who attended the ceremony were infected. They did not travel by bus but said they had been in close contact with the infected passenger.
The potential for airborne transmission in close confined spaces raises concern about the winter months, when people will be spending more time indoors, Marr said.
Her advice: “Avoid crowded indoor spaces where people are not wearing masks and the ventilation is poor.”