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, 23 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 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,” Dr. 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,” Dr. 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 on 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.
Frequently Asked Questions
Updated September 1, 2020
Why is it safer to spend time together outside?
- Outdoor gatherings lower risk because wind disperses viral droplets, and sunlight can kill some of the virus. Open spaces prevent the virus from building up in concentrated amounts and being inhaled, which can happen when infected people exhale in a confined space for long stretches of time, said Dr. Julian W. Tang, a virologist at the University of Leicester.
What are the symptoms of coronavirus?
- In the beginning, the coronavirus seemed like it was primarily a respiratory illness — many patients had fever and chills, were weak and tired, and coughed a lot, though some people don’t show many symptoms at all. Those who seemed sickest had pneumonia or acute respiratory distress syndrome and received supplemental oxygen. By now, doctors have identified many more symptoms and syndromes. In April, the C.D.C. added to the list of early signs sore throat, fever, chills and muscle aches. Gastrointestinal upset, such as diarrhea and nausea, has also been observed. Another telltale sign of infection may be a sudden, profound diminution of one’s sense of smell and taste. Teenagers and young adults in some cases have developed painful red and purple lesions on their fingers and toes — nicknamed “Covid toe” — but few other serious symptoms.
Why does standing six feet away from others help?
- The coronavirus spreads primarily through droplets from your mouth and nose, especially when you cough or sneeze. The C.D.C., one of the organizations using that measure, bases its recommendation of six feet on the idea that most large droplets that people expel when they cough or sneeze will fall to the ground within six feet. But six feet has never been a magic number that guarantees complete protection. Sneezes, for instance, can launch droplets a lot farther than six feet, according to a recent study. It’s a rule of thumb: You should be safest standing six feet apart outside, especially when it’s windy. But keep a mask on at all times, even when you think you’re far enough apart.
I have antibodies. Am I now immune?
- As of right now, that seems likely, for at least several months. There have been frightening accounts of people suffering what seems to be a second bout of Covid-19. But experts say these patients may have a drawn-out course of infection, with the virus taking a slow toll weeks to months after initial exposure. People infected with the coronavirus typically produce immune molecules called antibodies, which are protective proteins made in response to an infection. These antibodies may last in the body only two to three months, which may seem worrisome, but that’s perfectly normal after an acute infection subsides, said Dr. Michael Mina, an immunologist at Harvard University. It may be possible to get the coronavirus again, but it’s highly unlikely that it would be possible in a short window of time from initial infection or make people sicker the second time.
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 worshipers wore masks.
The paper in JAMA Internal Medicine does not describe the infected individual and says the person did not have symptoms until 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 on 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,” Dr. Cevik said.
The outdoor ceremony lasted two and a half 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, Dr. Marr said.
Her advice: “Avoid crowded indoor spaces where people are not wearing masks and the ventilation is poor.”