How the World Missed Covid-19’s Silent Spread

Symptomless transmission makes the coronavirus far harder to fight. But health officials dismissed the risk for months, pushing misleading and contradictory claims in the face of mounting evidence.

MUNICH — Dr. Camilla Rothe was about to leave for dinner when the government laboratory called with the surprising test result. Positive. It was Jan. 27. She had just discovered Germany’s first case of the new coronavirus.

But the diagnosis made no sense. Her patient, a businessman from a nearby auto parts company, could have been infected by only one person: a colleague visiting from China. And that colleague should not have been contagious.

The visitor had seemed perfectly healthy during her stay in Germany. No coughing or sneezing, no signs of fatigue or fever during two days of long meetings. She told colleagues that she had started feeling ill after the flight back to China. Days later, she tested positive for the coronavirus.

Scientists at the time believed that only people with symptoms could spread the coronavirus. They assumed it acted like its genetic cousin, SARS.

“People who know much more about coronaviruses than I do were absolutely sure,” recalled Dr. Rothe, an infectious disease specialist at Munich University Hospital.

But if the experts were wrong, if the virus could spread from seemingly healthy carriers or people who had not yet developed symptoms, the ramifications were potentially catastrophic. Public-awareness campaigns, airport screening and stay-home-if-you’re sick policies might not stop it. More aggressive measures might be required — ordering healthy people to wear masks, for instance, or restricting international travel.

Dr. Rothe and her colleagues were among the first to warn the world. But even as evidence accumulated from other scientists, leading health officials expressed unwavering confidence that symptomless spreading was not important.

In the days and weeks to come, politicians, public health officials and rival academics disparaged or ignored the Munich team. Some actively worked to undermine the warnings at a crucial moment, as the disease was spreading unnoticed in French churches, Italian soccer stadiums and Austrian ski bars. A cruise ship, the Diamond Princess, would become a deadly harbinger of symptomless spreading.

Interviews with doctors and public health officials in more than a dozen countries show that for two crucial months — and in the face of mounting genetic evidence — Western health officials and political leaders played down or denied the risk of symptomless spreading. Leading health agencies including the World Health Organization and the European Center for Disease Prevention and Control provided contradictory and sometimes misleading advice. A crucial public health discussion devolved into a semantic debate over what to call infected people without clear symptoms.

Behind The Curve: The Silent Spread of Covid-19

This series of articles examines the missteps, misunderstandings and missed warning signals that allowed Covid-19 to spread around the world.

The two-month delay was a product of faulty scientific assumptions, academic rivalries and, perhaps most important, a reluctance to accept that containing the virus would take drastic measures. The resistance to emerging evidence was one part of the world’s sluggish response to the virus.

It is impossible to calculate the human toll of that delay, but models suggest that earlier, aggressive action might have saved tens of thousands of lives. Countries like Singapore and Australia, which used testing and contact-tracing and moved swiftly to quarantine seemingly healthy travelers, fared far better than those that did not.

That night, Dr. Rothe tapped out an email to a few dozen doctors and public health officials.

“Infections can actually be transmitted during the incubation period,” she wrote.

Three more employees from the auto parts company, Webasto, tested positive the following day. Their symptoms were so mild that, normally, it’s likely that none would have been flagged for testing, or have thought to stay at home.

Dr. Rothe decided she had to sound the alarm. Her boss, Dr. Michael Hoelscher, dashed off an email to The New England Journal of Medicine. “We believe that this observation is of utmost importance,” he wrote.

Editors responded immediately. How soon could they see the paper?

The next morning, Jan. 30, public health officials interviewed the Chinese businesswoman by phone. Hospitalized in Shanghai, she explained that she’d started feeling sick on the flight home. Looking back, maybe she’d had some mild aches or fatigue, but she had chalked them up to a long day of travel.

“From her perspective, she was not ill,” said Nadine Schian, a Webasto spokeswoman who was on the call. “She said, ‘OK, I felt tired. But I’ve been in Germany a lot of times before and I always have jet lag.’”

When the health officials described the call, Dr. Rothe and Dr. Hoelscher quickly finished and submitted their article. Dr. Rothe did not talk to the patient herself but said she relied on the health authority summary.

Within hours, it was online. It was a modest clinical observation at a key time. Just days earlier, the World Health Organization had said it needed more information about this very topic.

What the authors did not know, however, was that in a suburb 20 minutes away, another group of doctors had also been rushing to publish a report. Neither knew what the other was working on, a seemingly small academic rift that would have global implications.

The second group was made up of officials with the Bavarian health authority and Germany’s national health agency, known as the Robert Koch Institute. Inside a suburban office, doctors unfurled mural paper and traced infection routes using colored pens.

Their team, led by the Bavarian epidemiologist Dr. Merle Böhmer, submitted an article to The Lancet, another premier medical journal. But the Munich hospital group had scooped them by three hours. Dr. Böhmer said her team’s article, which went unpublished as a result, had reached similar conclusions but worded them slightly differently.

Dr. Rothe had written that patients appeared to be contagious before the onset of any symptoms. The government team had written that patients appeared to be contagious before the onset of full symptoms — at a time when symptoms were so mild that people might not even recognize them.

The Chinese woman, for example, had woken up in the middle of the night feeling jet-lagged. Wanting to be sharp for her meetings, she took a Chinese medicine called 999 — containing the equivalent of a Tylenol tablet — and went back to bed.

Perhaps that had masked a mild fever? Perhaps her jet lag was actually fatigue? She had reached for a shawl during a meeting. Maybe that was a sign of chills?

After two lengthy phone calls with the woman, doctors at the Robert Koch Institute were convinced that she had simply failed to recognize her symptoms. They wrote to the editor of The New England Journal of Medicine, casting doubt on Dr. Rothe’s findings.

Editors there decided that the dispute amounted to hairsplitting. If it took a lengthy interview to identify symptoms, how could anyone be expected to do it in the real world?

“The question was whether she had something consistent with Covid-19 or that anyone would have recognized at the time was Covid-19,” said Dr. Eric Rubin, the journal’s editor.

“The answer seemed to be no.”

The journal did not publish the letter. But that would not be the end of it.

As Dr. Rothe and Dr. Hoelscher reeled from the criticism, Japanese doctors were preparing to board the Diamond Princess cruise ship. A former passenger had tested positive for coronavirus.

Yet on the ship, parties continued. The infected passenger had been off the ship for days, after all. And he hadn’t reported symptoms while onboard.

Immediately after Dr. Rothe’s report, the World Health Organization had noted that patients might transmit the virus before showing symptoms. But the organization also underscored a point that it continues to make: Patients with symptoms are the main drivers of the epidemic.

Once the Science article was published, however, the organization waded directly into the debate on Dr. Rothe’s work. On Tuesday, Feb. 4, Dr. Sylvie Briand, the agency’s chief of infectious disease preparedness, tweeted a link to the Science article, calling Dr. Rothe’s report flawed.

With that tweet, the W.H.O. focused on a semantic distinction that would cloud discussion for months: Was the patient asymptomatic, meaning she would never show symptoms? Or pre-symptomatic, meaning she became sick later? Or, even more confusing, oligo-symptomatic, meaning that she had symptoms so mild that she didn’t recognize them?

To some doctors, the focus on these arcane distinctions felt like whistling in the graveyard. A person who feels healthy has no way to know that she is carrying a virus or is about to become sick. Airport temperature checks will not catch these people. Neither will asking them about their symptoms or telling them to stay home when they feel ill.

The W.H.O. later said that the tweet had not been intended as a criticism.

One group paid little attention to this brewing debate: the Munich-area doctors working to contain the cluster at the auto parts company. They spoke daily with potentially sick people, monitoring their symptoms and tracking their contacts.

“For us, it was pretty soon clear that this disease can be transmitted before symptoms,” said Dr. Monika Wirth, who tracked contacts in the nearby county of Fürstenfeldbruck.

Dr. Rothe, though, was shaken. She could not understand why much of the scientific establishment seemed eager to play down the risk.

“All you need is a pair of eyes,” she said. “You don’t need rocket-science virology.”

But she remained confident.

“We will be proven right,” she told Dr. Hoelscher.

That night, Dr. Rothe received an email from Dr. Michael Libman, an infectious-disease specialist in Montreal. He thought that criticism of the paper amounted to semantics. Her paper had convinced him of something: “The disease will most likely eventually spread around the world.”

On Feb. 4, Britain’s emergency scientific committee met and, while its experts did not rule out the possibility of symptomless transmission, nobody put much stock in Dr. Rothe’s paper.

“It was very much a hearsay study,” said Wendy Barclay, a virologist and member of the committee, known as the Scientific Advisory Group for Emergencies. “In the absence of real robust epidemiology and tracing, it isn’t obvious until you see the data.”

The data would soon arrive, and from an unexpected source. Dr. Böhmer, from the Bavarian health team, received a startling phone call in the second week of February.

Virologists had discovered a subtle genetic mutation in the infections of two patients from the Munich cluster. They had crossed paths for the briefest of moments, one passing a saltshaker to the other in the company cafeteria, when neither had symptoms. Their shared mutation made it clear that one had infected the other.

Dr. Böhmer had been skeptical of symptomless spreading. But now, there was no doubt: “It can only be explained with pre-symptomatic transmission,” Dr. Böhmer said.

Now it was Dr. Böhmer who sounded the alarm. She said she promptly shared the finding, and its significance, with the W.H.O. and the European Center for Disease Prevention and Control.

Neither organization included the discovery in its regular reports.

A week after receiving Dr. Böhmer’s information, European health officials were still declaring: “We are still unsure whether mild or asymptomatic cases can transmit the virus.” There was no mention of the genetic evidence.

W.H.O. officials say the genetic discovery informed their thinking, but they made no announcement of it. European health officials say the German information was one early piece of an emerging picture that they were still piecing together.

  • Updated June 24, 2020

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The doctors in Munich were increasingly frustrated and confused by the World Health Organization. First, the group wrongly credited the Chinese government with alerting the German authorities to the first infection. Government officials and doctors say the auto parts company itself sounded the alarm.

Then, the World Health Organization’s emergency director, Dr. Michael Ryan, said on Feb. 27 that the significance of symptomless spreading was becoming a myth. And Dr. Maria Van Kerkhove, the organization’s technical lead on coronavirus response, suggested it was nothing to worry about.

“It’s rare but possible,” she said. “It’s very rare.”

The agency still maintains that people who cough or sneeze are more contagious than people who don’t. But there is no scientific consensus on how significant this difference is or how it affects the spread of virus.

And so, with evidence mounting, the Munich team could not understand how the W.H.O. could be so sure that symptomless spreading was insignificant.

“At this point, for us it was clear,” said Dr. Wendtner, the senior doctor overseeing treatment of the Covid-19 patients. “This was a misleading statement by the W.HO.”

The Munich cluster was not the only warning.

The Chinese health authorities had explicitly cautioned that patients were contagious before showing symptoms. A Japanese bus driver was infected while transporting seemingly healthy tourists from Wuhan.

And by the middle of February, 355 people aboard the Diamond Princess cruise ship had tested positive. About a third of the infected passengers and staff had no symptoms.

But public health officials saw danger in promoting the risk of silent spreaders. If quarantining sick people and tracing their contacts could not reliably contain the disease, governments might abandon those efforts altogether.

In Sweden and Britain, for example, discussion swirled about enduring the epidemic until the population obtained “herd immunity.” Public health officials worried that might lead to overwhelmed hospitals and needless deaths.

Plus, preventing silent spreading required aggressive, widespread testing that was then impossible for most countries.

“It’s not like we had some easy alternative,” said Dr. Libman, the Canadian doctor. “The message was basically: ‘If this is true, we’re in trouble.’”

European health officials say they were reluctant to acknowledge silent spreading because the evidence was trickling in and the consequences of a false alarm would have been severe. “These reports are seen everywhere, all over the world,” said Dr. Josep Jansa, a senior European Union health official. “Whatever we put out, there’s no way back.”

Looking back, health officials should have said that, yes, symptomless spreading was happening and they did not understand how prevalent it was, said Dr. Agoritsa Baka, a senior European Union doctor.

But doing that, she said, would have amounted to an implicit warning to countries: What you’re doing might not be enough.

While public health officials hesitated, some doctors acted. At a conference in Seattle in mid-February, Jeffrey Shaman, a Columbia University professor, said his research suggested that Covid-19’s rapid spread could only be explained if there were infectious patients with unremarkable symptoms or no symptoms at all.

In the audience that day was Steven Chu, the Nobel-winning physicist and former U.S. energy secretary. “If left to its own devices, this disease will spread through the whole population,” he remembers Professor Shaman warning.

Afterward, Dr. Chu began insisting that healthy colleagues at his Stanford University laboratory wear masks. Doctors in Cambridge, England, concluded that asymptomatic transmission was a big source of infection and advised local health workers and patients to wear masks, well before the British government acknowledged the risk of silent spreaders.

The American authorities, faced with a shortage, actively discouraged the public from buying masks. “Seriously people — STOP BUYING MASKS!” Surgeon General Jerome M. Adams tweeted on Feb. 29.

By early March, while the World Health Organization continued pressing the case that symptom-free transmission was rare, science was breaking in the other direction.

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