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Sunday, October 1, 2023

It’s Time to Talk About Covid-19 and Surfaces Again

Beth Kalb was worried about the pews. This summer, the century-old Catholic church she attends in a small town outside Minneapolis had, like many places, reopened its doors with new rituals of disinfection. Kalb had quickly noticed the side effects. The varnish on the pews had begun to wear, and the wood was often sticky with disinfectant, so the volunteer cleaners had started using soap and water to remove the tacky build-up. They were weeks in, and it had already come to cleaning off the cleaner. Plus, all those chemicals couldn’t be good for the people who were spritzing and wiping down the worship space after each use. As a nurse, Kalb knew the importance of handwashing, but this all seemed like a bit much. It was certainly too much for the wood.

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For Erin Berman, in Fremont, California, it was the books. In the spring, a federal project to help reopen libraries, called Realm, had commissioned tests to see how long the virus lasts on objects they lend. Researchers had borrowed materials from the library system in Columbus, Ohio, and applied an inoculum of the virus to them in a nearby lab to see how long it could remain infectious. They started mainly with books, measuring how much virus was left after a day or two, but in subsequent months, expanded to magazines and DVDs and USB drives. In August, a fourth round of tests addressed the question of placing books in stacks, rather than laying them out individually. Protected from light and drying air, the researchers were able to find virus particles on them after six days. On leather book covers, a fifth round of tests determined this month, the virus lasted at least eight days.

The Realm organizers emphasized that none of what they were reporting was guidance—it was research, meant to inform the staff at individual libraries who were deciding what to do with all those items gathering dust, and possibly germs, in people’s homes. However, they also noted it was not possible to disinfect every page of every book. So many library staffers, after seeing the data, were considering “book quarantines” that lasted a week or more.

Berman was aware of the practical issues raised by putting books in purgatory for so long, but she had a broader concern: that all this research was encouraging an undue fixation, or even a fear, of the objects librarians are meant to joyfully share with the public. It was hard to understand what those numbers—the number of days, the number of viral particles that remained—actually meant for spreading Covid-19 via books, but their very existence had generated anxiety among her coworkers. And she suspected that it was drawing focus away from all the other things she and her colleagues had to do to reopen safely—to reimagine a community space in which people could no longer safely linger, in which social connection would now be mediated by Plexiglass. “I started to get very frustrated. I’m thinking, ‘We’re librarians. We should be doing research,’” Berman says. “Of all the industries, we should not be operating in fear.”

For Emanuel Goldman, a virologist at Rutgers University, the worries began with the gentle nagging of his elderly mother-in-law. “She was telling me, ‘Wipe down this, wipe down that,’” he says. He had been obliging at the start of the pandemic. The requests seemed reasonable—a set of small acts to keep his household safer. He knew from other viruses that fomite spread—the technical term for passing on a virus via objects—was possible, and at that time the Centers for Disease Control and Prevention had little guidance on SARS-CoV-2. But as he delved into the research himself, he grew concerned. Despite all the fixation on how long and how much virus lasts on surfaces, there wasn’t much evidence at all that it was relevant to how Covid-19 actually spread. In July he laid out those concerns in a tersely worded commentary in The Lancet titled “Exaggerated risk of transmission of Covid-19 by fomites.”

“In my opinion, the chance of transmission through inanimate surfaces is very small, and only in instances where an infected person coughs or sneezes on the surface, and someone else touches that surface soon after the cough or sneeze (within 1–2 h),” he wrote. “I do not disagree with erring on the side of caution, but this can go to extremes not justified by the data.”

That was months ago, and since then the scientific evidence has tipped in Goldman’s favor. And yet, here we are all the same, wiping down pews and hiding away books, among countless other disinfection rituals molded by those early perceptions. “What’s done cannot be undone,” Goldman tells me now. “And it’s going to take a lot of time and effort to turn things around.”

In March, I wrote about what we knew at the time about our understanding of surface spread, which was very little. Nearly a year into the Covid-19 pandemic, it’s time to ask: What do we know now?

The first widely covered study on fomites and Covid-19, released as a preprint in March by researchers at the University of California, Los Angeles, the National Institutes of Health, and Princeton, was a look at how long the novel coronavirus lasted on different kinds of surfaces. At the time, little was known about how the virus was transmitted, so the question was important. Depending on the material, the researchers could still detect the virus after a few hours on cardboard, and after several days on plastic and steel. They were careful to say that their findings only went as far as that. They were reporting how quickly the virus decayed in a laboratory setting, not whether it could still infect a person or was even a likely mode of transmission.

But in the hazy panic of the time, many people had already taken up fastidious habits: quarantining packages at the door, bleaching boxes of cereal brought back from the store, wearing hospital booties outdoors. A single set of research results didn’t start those behaviors, but—along with other early studies finding the virus on surfaces in hospital rooms and on cruise ships—it appeared to provide validation.

Dylan Morris, a mathematical biologist at Princeton who coauthored the paper, recalls watching what he calls “the great fomite freakout” with frustration. The number of days the virus remained detectable on a surface in a lab wasn’t useful for assessing personal risk, he says, because in the real world, that amount would depend on how much there had been to start with and on environmental conditions that they did not test. Plus, the amount of remaining virus doesn’t tell us much about whether it could reasonably get into someone’s airways and cause an infection. “People really picked up on those absolute times to detectability,” he says. “Everyone wants to know the magical time when something becomes safe.” In subsequent research, he says he’s avoided giving hard temporal cutoffs.

Since March, additional studies have painted a picture that is much more subtle and less scary. But like that first study, each can be easily misinterpreted in isolation. One clear takeaway is that, given an adequate initial dose, some amount of the virus can linger for days or even weeks on some surfaces, like glass and plastic, in controlled lab conditions. Emphasis on controlled. For example, earlier this month, an Australian study published in Virology Journal found traces of the virus on plastic banknotes and glass 28 days after exposure. The reaction to that number felt to some like a replay of March: a single study with a bombshell statistic sparked new fears about touchscreens and cash. “To be honest, I thought that we had moved on from this,” says Anne Wyllie, a microbiologist at Yale University.

Of course, this was another laboratory study done with specific intentions. The study was done in the dark, because sunlight is known to quickly deactivate the virus, and it involved maintaining cool, favorable temperatures. Debbie Eagles, a researcher at Australia’s national science agency who coauthored the research, tells me that taking away those environmental variables allows researchers to better isolate the effect of individual factors, like temperature, on stability. “In most ‘real-world’ situations, we would expect survival time to be less than in controlled laboratory settings,” Eagles writes in an email. She advises handwashing and cleaning “high-touch” surfaces.

The second consistent finding is that there’s plenty of evidence of the virus on surfaces in places where infected people have recently been. Wherever there has recently been an outbreak, and in places where people are asked to quarantine or are treated for Covid-19, “there’s viral RNA everywhere,” says Chris Mason, a professor at Weill Cornell Medicine. That makes going out and swabbing a useful tool for keeping track of where the virus is spreading.

It’s tempting to piece those two elements together: If the virus is on the surfaces around us, and it also lasts for a long time in lab settings, naturally we should vigorously disinfect. But that doesn’t necessarily reflect what’s happening. In a study published in September in Clinical Microbiology and Infection, researchers in Israel tried to piece it all together. They conducted lab studies, leaving samples out for days on various surfaces, and found they could culture the remaining virus in tissue. In other words, it remained infectious. Then they gathered samples from highly contaminated environments: Covid-19 isolation wards at a hospital, and at a hotel used for people in quarantine. The virus was abundant. But when they tried to culture those real-world samples, none were infectious. Later that month, researchers at an Italian hospital reported similar conclusions in The Lancet.

In addition to environmental conditions, a confounding factor might be saliva, or the stuff that we often mean when we talk about droplets sticking onto surfaces. In her own research, Wyllie has studied how long certain viral proteins remain intact in saliva to help determine the reliability of Covid-19 spit tests. For her purposes, stability is a good thing. But some proteins have appeared to denature more quickly than others, she notes, suggesting the virus as a whole does not remain intact and infectious. That could be because saliva tends to be less hospitable to pathogens than the synthetic substances or blood serums often used in lab-based stability studies.

Consider, Wyllie says, the extraordinary chain of events that would need to happen to successfully spread SARS-CoV-2 on a surface. A sufficiently large amount of the virus would need to be sprayed by an infected person onto a surface. The surface would need to be the right kind of material, exposed to the right levels of light, temperature, and humidity so that the virus does not quickly degrade. Then the virus would need to be picked up—which you would most likely do with your hands. But the virus is vulnerable there. (“Enveloped” viruses like SARS-CoV-2 do not fare well on porous surfaces like skin and clothing.) And then it needs to find a way inside you—usually through your nose or your eye—in a concentration big enough to get past your mucosal defenses and establish itself in your cells. The risk, Wyllie concludes, is low. “I’ve not once washed my groceries or disinfected my bags or even thought twice about my mail,” she says.

Low risk is not, of course, no risk, she adds. There are high-touch objects that merit disinfection, and places like hospitals need clean rooms and furniture. People at high risk from Covid-19 may want to take extra precautions. But the best advice for breaking that object-to-nose chain, according to all the health experts I spoke with: Wash your hands.

Goldman, too, had come to similar conclusions months before all this additional research came out, and US public health guidance followed right along with him. Since his Lancet paper in July, the focus on fomites has waned, and has been replaced by a focus on person-to-person transmission through respiration. The shift was based on epidemiological evidence. Experts knew all along that droplets passed by sneezing, coughing, or speaking were likely an important mode of transmission—that’s just how respiratory viruses tend to move. Over time, it became clear that aerosols, which remain suspended in the air, can better explain why so many infections seemed to be passing between people who did not directly interact, but could have shared the same indoor air. That’s why public health officials now emphasize mask wearing and ventilation. The CDC’s most recently updated guidance, from early October, holds that “spread from touching surfaces is not thought to be a common way that Covid-19 spread.” For those reasons, or perhaps out of fatigue, the scrubbing became less scrupulous over the summer.

But not for everyone. “I think that one thing that has been tough about this pandemic is there has been such a strong initial message that gave people the wrong intuition,” says Morris, the Princeton researcher. For some people, and especially for institutions that were trying to reopen, liable to employees and visitors, priorities had been set based on what we knew back in the spring. It was also a way to show that they were doing something, Morris adds, even if it didn't do much. In July, The Atlantic’s Derek Thompson coined the term “hygiene theater” to describe the rash of corporate disinfection. It’s still around. It’s part of the reason why New York City has committed tens of millions of dollars to cleaning each subway car each night, why Airbnb requires “enhanced” cleaning from its landlords, why countless schools, stores, churches, and offices continue to emphasize disinfection. It’s why some libraries are quarantining books this fall for a week or more. It’s also a factor in what we are now less likely to do, a rationale for why many businesses no longer take cash and why playgrounds have often been among the last outdoor venues to reopen.

“There are bizarre policies that haven’t changed or adapted,” says Julia Marcus, an epidemiologist at Harvard Medical School. “It’s one thing for an individual to decide to stop bleaching their groceries. It’s much more difficult to steer the ship of an institution as the science evolves, with different levels of decisionmaking and different levels of health literacy and risk tolerance.”

What is it about fomites? There’s surely something psychological in the belief that we can “see” an invisible virus, manifesting as an object that we can quarantine, avoid, wipe down. That’s evident in how we think about the research, even. Recall the salt shaker in Germany? Or the elevator buttons in a Chinese high-rise? In New Zealand, there was that hypothesis that containers of frozen fish were responsible for an outbreak there. Some of those conclusions can be attributed to aerosol starting off as a dirty, alarmist word. Public health officials were searching for something, anything, to explain why groups of people who didn’t gather closely were becoming infected.

It’s impossible to rule out that some transmission could occur that way—and examples still come up, like a case in New Zealand possibly linked to a communal trash can—but most incidents now look like a case of shared air. Wyllie points to a friend who remains convinced they got the virus from a contaminated door handle. She thinks that’s unlikely, but for her friend, it’s an answer to a question of how they got sick that ambient virus floating in the air simply doesn’t offer. It’s a good story.

Sharon Streams, director of the Realm project, says she sympathizes with that demand for answers. The group’s research on library materials was conceived after the surface research in March. At the time, the talk was all fomites, at the time. Library employees wanted specifics to better understand how the virus interacts with the billions of materials they handle each year, many of which are currently marooned in people’s homes, exposed to who knows what. “They’re pulling their hair out about what is the appropriate level of quarantine,” she says.

Streams acknowledges that the conditions modeled in their experiments are based on a vague foundation. It’s hard to know whether the researchers started with a realistic dose of the virus, or whether the amount of it that remains on surfaces after a few days or hours would actually cause an infection. (The group’s latest research release, last week, included more language about aerosols and droplets being the likeliest modes of transmission.) But to her, that’s the point of gathering more data. And Streams points out that even if a weeklong quarantine looks like overkill to some virologists or health experts, quarantines and disinfection satisfy an emotional need that’s often overlooked. Much like the wiping down store shelves, church pews, or subway cars, cleaning policies are also about signaling which spaces are safe to come back to—that libraries are ready for visitors and employees. “‘Hygiene theater’ has been thrown around as a bad word, but they’re embracing it to show that we care about the people coming here,” she says. “They feel comforted.”

But communicating that point is difficult. Marcus points back to the original paper on surface spread in March: “They couched it appropriately. But even with those caveats, it spun into a lot of obsessive behaviors,” she says. Even seemingly benign procedures, like quarantining items, can wear people out over time. “There’s such a high level of tension in our lives and decisionmaking right now. We all need to feel some ease,” Marcus says. “For me, the question is, where are the low-risk areas where we can ease off the gas now that we know more about how transmission happens—which is overwhelmingly from being together in indoor environments? It’s not from a book that somebody sneezed on and brought to the library a week ago.”

Worrying about the small stuff exhausts people from focusing on things that do matter. There are all sorts of ways to imagine what might go wrong. Maybe a person feels so confident in the disinfection methods around them that they eat indoors without a mask, despite the much more substantial known risks. Or perhaps someone feels they don’t need to quarantine themselves after traveling because they wore disposable gloves and booties over their shoes on the plane. “When you ask more of people than what is needed, they grow tired of doing what actually matters,” Marcus says. Her advice: Keep it simple.

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That sort of clear, simple guidance is hard to come by. Since The Lancet publication, Goldman has become a consultant and therapist of sorts for people who are questioning the utility of overly rigorous disinfection, but who are unsure of what to make of the scientific evidence. He’s been in touch with administrators at a local school that planned to close once a week for “a deep clean,” but who weren’t paying attention to their ventilation systems. He has fielded inquiries from people who still leave their groceries out for days, and who barely leave the house, encouraging them to find a healthier balance. He may be able to change minds one at a time, he reasons, or at least help people put the risks in perspective. It worked, he says, on his mother-in-law. But behaviors are hard to shift, especially when the decision is made by committee. The tendency, in the absence of firm guidance to do otherwise, is to cater to the most cautious.

In Minnesota, Kalb, who is one of his acolytes, says her concerns about the pews, and the lack of evidence driving the deep cleaning, were carefully considered by the church reopening committee. But her fellow parishioners advised caution. The daily disinfection was part of a list of changes for safe reopening, including cordoning off rows for social distancing and a sign-up process to enable contact tracing. It was safest, the committee decided, to continue doing it all, much like every other nearby church and school and store was doing. After all, Kalb couldn’t point to a specific study that said fomite transmission was never happening. And there was news going around of an outbreak at a church in Texas. “It was like, OK, we don’t want to be that church,” she says. The church now uses a misting machine to spray disinfectant, which requires less active wiping.

It’s tempting, in other words, to play it conservatively, says Berman, the librarian. “Some of it is just making sure the employees or the public feel safe,” she says, and she sees the benefits of disinfecting library surfaces that get a lot of use. But she points out that institutions have the power to alter our perception of safety, cutting through the ambiguity of risk by offering clear guidance. Holding out these scientific conclusions—the number of days the virus lasts on every imaginable type of library material surface—had done just the opposite, she believed, producing more fear than empowerment.

Like so many decisions about risk and public safety in this pandemic, the burden had been displaced onto people like her, a librarian, not a virologist. She marveled at how much effort she was personally expending trying to educate herself and the people around her about the risk of books as fomites, when there was so much else to worry about. And, well, now she had done the research, and she knew the biggest risk in a library is the risk of sharing the same air, not touching the same book. Wouldn’t it be nice if someone with more authority would just come out and say so? “There’s so much fear out there,” she says. “I don’t want to put anyone at undue risk, but I want us to reopen.”

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