Covid-19 Rarely Infects Through Surfaces

Feature ZHAI YUJIA/CHINA NEWS SERVICE VIA GETTYZHAI YUJIA/CHINA SERVICE NEWS Workers spray disinfectant on a street in Shijiazhuang, China, in January 2020.

— houses, buses, churches, schools and shops — should clean and disinfect surfaces, espe- COVID-19 RARELY INFECTS cially those that are frequently touched. Dis- infectant factories worked around the clock THROUGH SURFACES. SO WHY to keep up with heavy demand. But Goldman, a microbiologist at Rutgers ARE WE STILL DEEP CLEANING? New Jersey Medical School in Newark, decided to take a closer look at the evidence around The coronavirus behind the pandemic can linger on fomites. What he found was that there was lit- doorknobs and other surfaces, but these aren’t a major tle to support the idea that SARS-CoV-2 passes from one person to another through contam- source of infection. By Dyani Lewis inated surfaces. He wrote a pointed commen- tary for The Lancet Infectious Diseases in July, arguing that surfaces presented relatively little risk of transmitting the virus2. His conviction has only strengthened since then, and Gold- hen Emanuel Goldman went showed that the coronavirus SARS-CoV-2 can man has long since abandoned the gloves. to his local New Jersey super- persist on plastic and stainless steel for days1. Many others reached similar conclusions. market last March, he didn’t That triggered startling headlines and a slew In fact, the US Centers for Disease Control and take any chances. Reports of of advice on how to decontaminate everything Prevention (CDC) clarified its guidance about COVID-19 cases were popping from doorknobs to groceries. It also seemed to surface transmission in May, stating that this up across the United States, so confirm guidance issued by the World Health route is “not thought to be the main way the he donned gloves to avoid con- Organization (WHO) in February that the virus virus spreads”. It now states that transmission taminated surfaces and wore a that causes COVID-19 can spread through con- through surfaces is “not thought to be a com- Wmask to prevent him inhaling tiny virus-laden taminated surfaces, known as fomites. mon way that COVID-19 spreads”. droplets from fellow shoppers. Neither gloves By May, the WHO and health agencies As evidence has accumulated over the nor masks were recommended at the time. around the world were recommending that course of the pandemic, scientific understand- Then, at the end of March, a laboratory study people in ordinary community settings ing about the virus has changed. Studies and

investigations of outbreaks all point to the facilities for places the virus could be lurking. at the Assuta Ashdod University Hospital in majority of transmissions occurring as a result And it seemed to be everywhere. Israel, and his colleagues swabbed personal of infected people spewing out large droplets In medical facilities, personal items such as items and furniture in hospital isolation units and small particles called aerosols when they reading glasses and water bottles tested posi- and rooms at a quarantine hotel. Half of the cough, talk or breathe. These can be directly tive for traces of viral RNA — the main way that samples from two hospitals and more than inhaled by people close by. Surface transmis- researchers identify viral contamination. So, one-third of samples from the quarantine sion, although possible, is not thought to be too, did bed rails and air vents. In quarantined hotel were positive for viral RNA. But none of a significant risk. households, wash basins and showers har- the viral material was actually able to infect But it’s easier to clean surfaces than improve boured the RNA, and in restaurants, wooden cells, the researchers reported7. ventilation — especially in the winter — and chopsticks were found to be contaminated. Indeed, researchers have struggled to iso- consumers have come to expect disinfec- And early studies suggested that contamina- late viable virus from any environmental sam- tion protocols. That means that govern- tion could linger for weeks. Seventeen days ples, not just fomites. In the only study that has ments, companies and individuals continue after the Diamond Princess cruise ship was succeeded, researchers grew virus particles to invest vast amounts of time and money in vacated, scientists found viral RNA on surfaces from hospital air samples collected at least deep-cleaning efforts. By the end of 2020, in cabins of the 712 passengers and crew mem- 2 metres from a person with COVID-19 (ref. 8). global sales of surface disinfectant totalled bers who tested positive for COVID-19 (ref. 3). Nevertheless, scientists warn against US$4.5 billion, a jump of more than 30% over drawing absolute conclusions. “Just because the previous year. The New York Metropolitan viability can’t be shown, it doesn’t mean that Transit Authority (MTA), which oversees sub- there wasn’t contagious virus there at some ways and buses and lost billions of dollars in point,” says epidemiologist Ben Cowling at the passenger revenue in 2020, spent $484 million What we really, really University of Hong Kong. last year in its response to COVID-19, including value is epidemiological Human exposure studies of other patho- enhanced cleaning and sanitization, according gens provide additional clues about fomite to a spokesperson. investigations of transmission of respiratory viruses. In 1987, Part of the problem is that specialists can’t transmission patterns.” researchers at the University of Wisconsin— rule out the possibility of fomite transmis- Madison put healthy volunteers in a room sion, and the guidance from many health to play cards with people infected with a agencies about how to deal with surfaces has common-cold rhinovirus9. When the healthy been unclear as the science has changed. In But contamination with viral RNA is not nec- volunteers had their arms restrained to stop November, Chinese authorities introduced essarily cause for alarm, says Goldman. “The them touching their faces and prevent them guidelines requiring disinfection of imported viral RNA is the equivalent of the corpse of the transferring the virus from contaminated sur- frozen-food packages. And the CDC directs virus,” he says. “It’s not infectious.” faces, half became infected. A similar number people to a comprehensive list of agents that To address that part of the equation, of volunteers who were unrestrained also kill SARS-C0V-2 and says: “Frequent disinfec- researchers began testing whether coronavi- became infected. In a separate experiment, tion of surfaces and objects touched by mul- rus samples left for days on various surfaces cards and poker chips that had been handled tiple people is important.” could infect lab-grown cells. One study in April and coughed on by sick volunteers were taken Experts say that it makes sense to recom- found that the virus remained infectious on to a separate room, where healthy volunteers mend hand washing, but some researchers are hard surfaces such as plastic and stainless were instructed to play poker while rubbing pushing back against the focus on surfaces. In steel for 6 days; on bank notes, it lasted for their eyes and noses. The only possible mode December, engineer Linsey Marr at Virginia 3 days; and on surgical masks, at least 7 days4. of transmission was through the contaminated Tech in Blacksburg co-wrote an opinion article A later study announced that viable virus was cards and chips; none became infected. The for The Washington Post imploring people to present on skin for up to 4 days, but on clothes combination of experiments provided strong ease up on cleaning efforts. “It’s become clear it survived for less than 8 hours5. And others evidence that rhinoviruses spread through the that transmission by inhalation of aerosols — found infectious virus on library books bound air. But such studies are considered unethical the microscopic droplets — is an important in natural and synthetic leather after 8 days6. for SARS-CoV-2, because it can kill. if not dominant mode of transmission,” says Although it’s probably rare, says Cowling, Marr, who studies airborne disease transmis- Unrealistic conditions transmission through surfaces can’t be ruled sion. Excessive attention on making surfaces Although these types of experiment demon- out. “It just doesn’t seem to happen that much, pristine takes up limited time and resources strate that the coronavirus can survive on as far as we can tell.” that would be better spent on ventilation or surfaces, this doesn’t mean that people are Estimates of transmission based on levels of the decontamination of the air that people catching it from surfaces such as doorknobs. viral RNA persisting in the environment seem breathe, she says. Goldman and others caution against reading to bear this out. From April to June, environ- too much into virus-survival studies, because mental engineer Amy Pickering then at Tufts Virus RNA can mislead most don’t test conditions that exist outside University in Medford, Massachusetts, and her The focus on fomites — rather than aerosols the lab. “They were experiments that started colleagues took weekly swabs of indoor and — emerged at the very beginning of the coro- out with humongous amounts of virus, noth- outdoor surfaces around a town in Massachu- navirus outbreak because of what people knew ing that you would encounter in the real world,” setts. On the basis of the levels of RNA contami- about other infectious diseases. In hospitals, he says. Other tests have used mock saliva nation and how often people touched surfaces pathogens such as methicillin-resistant Staph- and controlled conditions such as humidity such as doorknobs and buttons at pedestrian ylococcus aureus, respiratory syncytial virus and temperature, all of which widen the gulf crossings, the team estimated10 that the risk and norovirus can cling to bed rails or hitch a between experimental and real-world condi- of infection from touching a contaminated ride from one person to the next on a doctor’s tions, says Goldman. surface is less than 5 in 10,000 — lower than stethoscope. So as soon as people started fall- Only a handful of studies have looked for estimates for SARS-CoV-2 infection through ing ill from the coronavirus, researchers began viable virus outside the lab. Tal Brosh-Nissi- aerosols, and lower than surface-transmission swabbing hospital rooms and quarantine mov, who heads the infectious-diseases unit risk for influenza or norovirus.

Feature and it also is probably not reducing your exposure that much,” she says. Instead, reasonable hand hygiene, as well as wearing a mask and social distancing to reduce exposure from close contacts is a better place to focus efforts. The WHO updated its guidance on 20 Octo- ber, saying that the virus can spread “after infected people sneeze, cough on, or touch surfaces, or objects, such as tables, doorknobs and handrails”. A WHO spokesperson told Nature that “there is limited evidence of transmission through fomites. Nonetheless, fomite transmission is considered a possible mode of transmission, given consistent find- ing of environmental contamination, with positive identification of SARS-CoV-2 RNA in the vicinity of people infected with SARS-CoV-2.” The WHO adds that “disinfection practices are important to reduce the potential for COVID-19 virus contamination”.

The CDC did not respond to Nature’s queries GALAI/GETTY NOAM Sanitization of public transport in New York City cost hundreds of millions of dollars in 2020. about inconsistencies in its statements about the risks posed by fomites. “Fomite transmission is possible, but it just report, which has not been released in detail, The conundrum facing health authorities, seems to be rare,” says Pickering, who is now that a worker at a frozen-food business in the says Marr, is that definitively ruling out sur- at the University of California, Berkeley. “A lot northern port city of Tianjin became infected face transmission is hard. Authorities can be of things have to fall into place for that trans- after handling contaminated packaging of reluctant to tell people not to be cautious. “You mission to happen.” frozen pork imported from Germany. But the never want to say, ‘Oh, don’t do that,’ because That might explain why a global compari- WHO and other experts have disputed claims it can happen. And you know, we should follow son of government interventions to control that people can be infected through the food the precautionary principle,” she says. the pandemic in its early months found that chain in this manner. Despite the evolving evidence, the pub- cleaning and disinfection of shared surfaces Cowling says that more detailed investi- lic might have grown to expect extra levels ranked one of the least effective at reducing gations are needed, carefully tracking who of sanitization after the early months of the transmission11. Social distancing and travel infects whom, and what surfaces and spaces pandemic. When the New York MTA surveyed restrictions, including lockdowns, worked they shared around the time of infection. passengers in late September and early Octo- the best. “What we really, really value is epidemiolog- ber, three-quarters said that cleaning and ical investigations of transmission patterns, disinfecting made them feel safe when using Messy data whether it’s in households or workplaces or transport. That leaves researchers sorting through messy elsewhere,” he says. “I don’t think we’ve been Goldman continues to wear a cloth mask epidemiological data about how the virus doing enough of that.” when he leaves home, but when it comes to the spreads. Hundreds of studies of COVID-19 possibility of catching the coronavirus from transmission have been published since the The greatest threat a contaminated surface, he doesn’t take any pandemic began, yet there is thought to be Armed with a year’s worth of data about coro- special precautions. “One of the ways we pro- only one that reports transmission through a navirus cases, researchers say one fact is clear. tect ourselves is by washing our hands,” he says, contaminated surface, by what it termed the It’s people, not surfaces, that should be the “and that applies pandemic or no pandemic.” snot–oral route. According to the report, a main cause for concern. Evidence from super- person with COVID-19 in China blew his nose spreading events, where numerous people are Dyani Lewis is a science journalist in with his hand and then pressed a button in his infected at once, usually in a crowded indoor Melbourne, Australia. apartment building elevator. A second resi- space, clearly point to airborne transmission, 1. van Doramalen, N. et al. N. Engl. J. Med. 382, 1564–1567 dent in the building then touched the same says Marr. “You have to make up some really (2020). button and flossed with a toothpick imme- convoluted scenarios in order to explain 2. Goldman, E. Lancet Infect. Dis. 20, 892–893 (2020). 3. Moriarty, L. F. et al. Morb. Mortal. Wkly Rep. 69, 347–352 diately after, thereby transferring the virus superspreading events with contaminated (2020). 12 from button to mouth . But without genome surfaces,” she says. 4. Chin, A. W. H. et al. Lancet Microbe 1, E10 (2020). sequences of the viruses infecting each per- Hand washing is crucial, says Marr, because 5. Harbourt, D. E. et al. PLoS Negl. Trop. Dis. 14, e0008831 (2020). son, transmission through another unknown surface transmission can’t be ruled out. But 6. The REALM Project. Test 5: Natural attenuation as a person couldn’t be ruled out. it’s more important to improve ventilation decontamination approach for SARS-CoV-2 on textile In one other case, eight people in China are systems or to install air purifiers than to ster- materials (REALM, 2020); available at go.nature. com/3t1eycg thought to have been infected after stepping ilize surfaces, she says. “If we’ve already paid 7. Ben-Shmuel, A. et al. Clin. Microbiol. Infect. 26, 1658–1662 in sewage containing the virus on the street attention to the air and we have some extra (2020). and then walking the contamination into time and resources, then yes, wiping down 8. Lednicky, J. A. et al. Int. J. Infect. Dis. 100, 476–482 (2020). 13 9. Dick, E. C. et al. J. Infect. Dis. 156, 442–448 (1987). their homes . those high-touch surfaces could be helpful,” 10. Harvey, A. P. et al. Environ. Sci. Technol. Lett. https://doi. Despite the rarity of published examples she says. org/10.1021/acs.estlett.0c00875 (2020). of fomite transmission, Chinese authorities Households can also ease up, says Pickering. 11. Haug, N. et al. Nature Human Behav. 4, 1303–1312 (2020). 12. Xie, C. et al. BMC Public Health 20, 1202 (2020). require that imported frozen food be disin- Quarantining groceries or disinfecting every 13. Yuan, J. et al. Clin. Infect. Dis. https://doi.org/10.1093/cid/ fected. The change in guidelines followed a surface is going too far. “That’s a lot of work ciaa1494 (2020).