The death of two elderly cruise ship passengers infected with a novel coronavirus, announced by the Japanese government on Thursday, has health experts pointing to the flulike potential spread of the COVID-19 illness worldwide, and the dangers of quarantines in closed environments like cruise ships.

The ships have emerged as the ill-fated petri dishes of the novel coronavirus outbreak. The largest outbreak site outside of China is the Diamond Princess anchored in Japan, currently counting more than 600 passengers diagnosed with COVID-19. Cambodia is threatened with an outbreak from passengers disembarked from a second cruise ship, the Westerdam, which turned out to have contained at least one infected passenger, an 83-year-old American woman.

The Diamond Princess carried 3,700 passengers and crew when it was quarantined two weeks ago. Since then, more than 600 people confirmed with the illness have been taken off for medical care, more than 300 Americans have flown home to mandatory quarantine, and about 600 mostly elderly passengers who tested negative were let off the ship on Thursday. “Several hundred” more are expected to disembark on Friday, according to Princess Lines, which offered everyone aboard a full refund on Feb. 9. Canada is also arranging to fly its passengers home, and 11 Israelis will head into medical isolation at Sheba Medical Center.

“Obviously there have been more transmissions than anticipated,” said World Health Organization Health Emergencies Program executive director Mike Ryan, asked about the cruise ship outbreak on Tuesday. ”Sometimes there are environments in which viruses can more easily spread.”

The massive outbreak in China’s Hubei province and medical reports looking at the spread of infections there point to COVID-19 spreading most like influenza, said University of Iowa’s Stanley Perlman. The flu virus is readily distributed in airborne particles by sneezing, coughing people in the middle stages of their symptoms, in contrast to the 2003 SARS outbreak, where people were most infectious during the severe coughing that came in the late stages of infection. Understanding the rapid spread of cases on the Princess Diamond cruise ship could help further explain how the virus has spread by air in the wider outbreak.

On Wednesday, WHO announced it was providing medical supplies and advice to Cambodia’s Ministry of Health following the discovery that an 83-year-old American woman who had disembarked from the Westerdam cruise ship in that country had tested positive for COVID-19.

And the day before, the CDC announced that the 100 or more US passengers still aboard the Diamond Princess or in Japanese hospitals couldn’t enter the US until they had undergone 14 days of quarantine after leaving the ship, or else undergo a mandatory 14-day quarantine on US soil.

“Because of their high-risk exposure, there may be additional confirmed cases of COVID-19 among the remaining passengers onboard the Diamond Princess,” said the CDC announcement. The same day, 79 new cases were announced onboard the ship.

As of Thursday morning, there are some 75,752 cases of confirmed coronavirus worldwide. More than 99% of the cases are in China, where authorities have again revised their case definition to exclude cases not confirmed by lab reports, leading to lower daily case numbers and drawing complaints from outside public health experts. The cases now include 2,130 deaths, only 8 of them outside China - including the two patients in their eighties from the Diamond Princess.

“It’s very easy in retrospect to question public health decisions,” said WHO’s Ryan. “It will be very important to study this particular event and see what the issues have been that have led to the transmission to the people that have been on that ship.”

But even with only a little hindsight, experts in respiratory disease transmission in confined settings say some lessons are apparent from the saga of the Diamond Princess and Westerdam.

Cruise ships can’t filter air well enough to stop the spread of viruses

“Get off that ship - there are a lot better places to isolate people,” Purdue University's Qingyan Chen, an expert on ventilation during virus outbreaks, told BuzzFeed News. “In ships, you cannot filter the air well enough to stop viruses.”

Health experts have warned about the potential for cruise ship outbreaks for years. A ship’s ventilation system, which relies on recirculated air filtered by medium-strength air filters, is an efficient way of spreading virus particles from room to room aboard a ship, said Chen. In a 2015 study, he and his colleagues looked at the spread of flu aboard cruise ships, finding that one infected person would typically lead to more than 40 cases a week later on a 2,000 passenger cruise, with transmission occurring through the ventilation system. In contrast, on land, the coronavirus seems to have a reproductive rate of two new cases per infected person, which would lead to three new cases in that time.

A 2018 CDC study of two Alaskan cruise ships that suffered flu outbreaks found that 83% of 410 passengers on the two ships were infected with some respiratory illness within the second week of the cruises, with how soon passengers boarded the ship presenting the biggest determinant of their risk.

On the Diamond Princess, 10 passengers were diagnosed with coronavirus on Feb. 4, two weeks after an infected passenger set foot on the ship. Since flu viruses are about the same size as coronaviruses, roughly 120 to 125 nanometers wide, and the ship’s ventilation system air filters can only screen out particles 1,000 nanometers across, the disease could spread even if the infected passengers were isolated, Chen said. The current infection rate aboard the Diamond Princess, where 621 out of 3,700 passengers and crew are diagnosed five weeks after the start of a trip, doesn’t look too surprising, he said, following that model.

At this point, he added, the entire ventilation system is likely filled with the virus, even if they were to switch to circulating only fresh air. “It’s really kind of too late for the Diamond Princess, right now,” he said.

Some experts say the cruise ship quarantines were botched

Leaving aside the spread of viruses through the air shafts, cruise ships are notorious for spreading illnesses. The CDC has issued warnings related to cruise ships and norovirus, and both the Diamond Princess and Westerdam cases appear mishandled to outside observers. Close quarters, the coming and going of new passengers, and eating together in communal settings all make ships ripe for passing around illnesses.

“A cruise ship is not an ideal place for a quarantine,” epidemiologist Don Milton of the University of Maryland, who studies how coronaviruses spread among university dorm rooms, told BuzzFeed News.

Even so, the quarantine on the Diamond Princess was not rigorous, according to one infectious disease expert, Kentaro Iwata of Kobe University Hospital, who went aboard on Tuesday to help advise health officials on how to prevent the virus’s spread. In isolation himself to protect his family from possible infection, he released a YouTube video saying that health ministry officials and crew members mingled and ate together on the Diamond Princess, with some in protective gear and some not, crossing between “green” infection-free zones on the ship and “red” suspect ones, creating ripe conditions for infections to walk off the ship.





YouTube video of Kentaro Iwata of Kobe University Hospital.

“The cruise ship was completely inadequate in terms of infection control,” Iwata said on the video, posted on Tuesday.

Japanese health ministry officials defended their quarantine aboard the boat but acknowledged that three ministry personnel sent aboard the ship had become infected.

Communication about lab testing for the virus was also botched: Of 328 passengers flown to the US on Tuesday, 14 turned up infected in buses on the way to the airport and had to fly home in a separate section of a cargo aircraft, according to William Walters at the US Department of State’s Bureau of Medical Services.

“Once they were on the bus, we received information about a lab test that had been done two or three days earlier,” Walters said at a news briefing.

And the Westerdam passenger who disembarked in Cambodia was only detected as sick when she was screened at an airport in Malaysia, meaning more sick people from the ships might be running loose, undetected.

Staying indoors carries its own risk

Even dorm rooms and hospitals aren’t perfect places to stop an infection, said Milton. “It’s not easy to find a place to put 3,000 potentially ill people, to transport them, to feed and house them in isolation quickly.”

Hospital isolation wards equipped with high-quality filters that can catch 99% of virus particles are no guarantee of stopping the spread of viruses indoors. In a 2015 outbreak of the MERS coronavirus in South Korea that led to 39 deaths, doctors detected virus particles in the corridors outside hospital rooms equipped with “negative pressure” air conditioning designed to only pull in air from outside the room.

Those high-quality air filters that can screen out virus particles block a lot of airflow, meanwhile, making them impractical to use on a large scale because they require more energy than conventional air conditioning systems can generate.

“The real problem is that indoor air just tends to accumulate viruses,” said Milton. “Maybe what they should have done is have everyone sleep outside. There’s plenty of fresh air there.”

One real unknown in how to best isolate people in the coronavirus outbreak is the open question of the infectiousness of people in the early stages of the virus, when they are likely shedding virus particles. If the early stages of a case aren’t very infectious, then running a lot of air through cheaper air filters that are 80% effective at catching viruses would be just as effective, said Milton, and actually feasible for hotel or dorm room medical isolation.

“I really worry about taxis and personal cars, taking people from the airport,” he added. Infected taxi drivers have been reported in Thailand and in Japan, and a Taiwanese taxi driver with no known contact with coronavirus patients died of COVID-19 on Saturday. In warm climates, the air conditioning is recirculating air all day.

“The driver and passengers are really just breathing the same air all day,” he said, and car air filters are not particularly effective at screening viruses.

Ventilation is slightly better on planes

On the other hand, the State Department’s decision to send the just-diagnosed Diamond Princess passengers on an airplane was a reasonable one, said Chen, because of airflow aboard aircraft.

Airplanes rely on both high-quality air filters and are designed to circulate air within cabin sections. Loading the infected people in a rear-closed section of the plane and giving them medical masks to wear would be “very effective to minimize risks,” said Chen. (The CDC objected to the transfer of the 14 infected patients nevertheless, the Washington Post reported on Thursday.)

From the SARS experience, air carriers should use alcohol wipes to carefully wipe down surfaces on planes that might have held infected passengers, to prevent infecting passengers who get on the plane later. Headrests, armrests, fold-out trays, and anywhere else people regularly put their hands need extra attention.

“The toilets should be cleaned as often as possible,” Chen added. “It’s really important to keep the lid closed when you flush.” Even though airplane toilets are effectively a kind of vacuum, their action is so vigorous it can send virus particles upward to cover the hands and surfaces in the restroom cabin if the lid is open. “People don’t like to talk about it but it is really these small details that matter.”

A key message from past outbreaks is that people can do things to keep their risk lower, said Milton. The CDC recommends washing your hands frequently and avoiding contact with sick people, just like in a normal flu season.

“People have trouble with the fear factor - ‘airborne’ sounds scary, but flu is airborne, and we face it all the time,” said Milton. Medical isolation of infected patients with ventilation that doesn’t spread viruses to uninfected people will doubtless be one key to stopping outbreaks, he suggested.

“We can all Monday-morning-quarterback what happened in Japan, but I don’t know what I would have done in their shoes,” he added. “We don’t have the transmission data quite yet to have all the right answers.”