If you read anything about SARS-CoV-2, the novel coronavirus that causes COVID-19, transmission is described as person-to-person via direct contact and respiratory droplets, with fomites as a less common possibility. Whether it is airborne is, well, up in the air.
But what everyone really wants to know is how you translate this information into practical recommendations. Are the widespread use of masks, frequent hand hygiene and disinfection of surfaces, and social distancing at six feet from others necessary? Many emergency physicians and other high-risk health care workers have gone further, devising elaborate decontamination rituals, and some even electing to live apart from their families. Given reports of infected health care workers, their concern is not unwarranted.
Health care workers don't want to get infected, but even more importantly, they don't want to bring the virus home to their families. Making matters worse, it has become increasingly apparent that up to 44 percent of COVID-19 cases are transmitted by asymptomatic or presymptomatic people. Infectiousness is thought to start 2.3 days prior and peak 0.7 days prior to symptom onset. (Nat Med. 2020 Apr 15. https://go.nature.com/3f2vi4V.)
Lessons from Case Clusters
As expected, transmission between close household contacts and family members is common, presumably due to close direct contact, face-to-face interactions, and possibly shared contaminated surfaces. (See tables 1 and 2 online: https://bit.ly/CornonavirusTransmission.)
Close contact, especially in enclosed indoor spaces, is a recurring risk factor. The European Centre for Disease Prevention and Control defines high-risk exposure as direct physical contact—being with the person in a closed environment for more than 15 minutes, having face-to-face contact within six feet for more than 15 minutes, and being on an aircraft within two seats in any direction. Prior studies of adults show only slightly more respiratory droplets produced with coughing compared with talking. (J R Soc Interface. 2009;6 [Suppl 6]:S703; https://bit.ly/2YiqLpl; J Epidemiol. 2013;23:251; https://bit.ly/3aQl8ky.) Another risk factor highlighted is singing or vocalizing in close proximity to others, as seen by the choir practice cluster.
Dining with someone who is infected may be especially risky due to respiratory droplets expelled while combining eating and talking. Contact tracing revealed several patients whose sole exposure was a shared meal or sitting near an infected person in a restaurant or at a banquet. Dining face-to-face from a close distance combined with conversation is likely even a higher risk.
Outbreaks at sporting events, spring break trips, cruises, and meat processing plants, reinforce the importance of avoiding large gatherings and crowded conditions. Religious gatherings, birthday parties, and funerals have figured prominently in reported clusters. Several factors come together at these events, including large numbers of attendees, crowded and enclosed spaces, singing and vocalizing, and the tendency to shake hands or embrace in greeting.
Secondary Attack Rates
The evidence for secondary attack rates reported in the medical literature (see table 3 online) for family contacts, close contacts, and health care workers is not very clear. Attack rates are likely to vary widely by pandemic timing, and secondary attack rates are higher early on because of reduced awareness. Family members unsurprisingly have the highest secondary attack rate at approximately 10-30 percent. Spouses have a higher rate, children are less affected than adults, and secondary attack is reduced if the index patient quarantines separately from the family immediately upon becoming symptomatic. (Preprints with The Lancet. 2020 Mar 31. https://bit.ly/2y2FsCh; Chinese J Preventive Medicine. 2020:54 [Epub ahead of print]; (Clin Infect Dis. 2020 Apr 17.)
The U.S. Centers for Disease Control and Prevention recently expanded sentinel symptoms beyond fever, cough, and shortness of breath to include chills and shaking, myalgias, headache, sore throat, and loss of sense of taste or smell. (https://bit.ly/2VNPwIh.) The small amount of data currently available shows household member secondary attack rates of 8-16 percent (although much higher in closer quarters).
Secondary attack rates in close contacts are generally less than five percent unless there is a high-risk situation such as a shared meal or enclosed environment such as a cruise ship. Likelihood of transmission is increased with longer duration and higher-risk contact with currently symptomatic patients.
The few reports of health care worker secondary attack rates estimated through contact tracing (when a patient was not initially diagnosed and PPE use was inappropriate) are mostly zero, which contradicts reports of 20 percent of Italian health care workers becoming infected (Lancet. 2020;395:1225; https://bit.ly/2Yh1D2b), 50 positive health care workers identified in King County, WA, between Feb. 28 and March 13, 2020 (JAMA. 2020 Apr 17. https://bit.ly/2SjDbt8), identification of 9282 U.S. health care worker COVID-19 cases reported to the CDC from Feb. 12 to April 9, 2020 (MMWR. 2020;69:477; https://bit.ly/2WbNMYk), and 18 percent positive (282/1533) of U.K. symptomatic health care workers tested over a two-week period. (Euro Surveill. 2020;25; https://bit.ly/2Si4yDQ.)
Some health care workers may be exposed through community contacts, although the CDC study of U.S. health care workers found that 55 percent reported health care setting exposure only, 27 percent household exposure, 13 percent community exposure, and five percent multiple settings. (MMWR. 2020;69:477; https://bit.ly/2WbNMYk.)
There's hope. The proportion of new COVID-19-positive cases in China among health care workers decreased from 5.72 percent from Jan. 11 to Jan. 20, 2020, to 2.68 percent from Feb. 1 to Feb. 11, 2020; this was attributed to better PPE availability, enhanced vigilance, and improved self-protection knowledge and experience. (Front Med. 2020 Mar 23. https://bit.ly/2VLIwvn.)
Fomite transmission of respiratory viruses is a known phenomenon, which is why we have recommendations for meticulous hand hygiene, not touching one's face, and frequent surface disinfection. There are few to no clear cases of COVID-19 fomite transmission found in the literature. A workplace investigation found the only contact between the transmitter and recipient of the virus to be when, while sitting back to back in a canteen, one turned around to the other and asked for the salt. (Preprints with The Lancet. 2020 Mar 31. https://bit.ly/2y2FsCh.)
An epidemiologic investigation into the case of a woman in Charlotte, NC, who had left her house only once in three weeks to go to the pharmacy concluded that she was infected by touching the pharmacy keypad. (WCNC, Charlotte, NC, April 21, 2020; https://bit.ly/3d0MEO4.) On the other hand, an article about a case cluster from a carnival party in Germany found scant evidence of the virus being transmitted via the surfaces of door handles, smartphones or other objects. (The Guardian. 9 April. https://bit.ly/2Sk2LOI.) It may be difficult to answer this one. It is hard to say whether the virus was passed via a salt-shaker fomite or close-contact respiratory droplets.
Multiple studies have reported on swabs of patients' rooms and hospital areas for COVID-19 viral RNA, finding more samples positive in the ICU than the general ward, extensive contamination of COVID-19 patient rooms before cleaning but not after cleaning, and mixed findings on testing health care worker PPE. (Emerg Infect Dis. 2020;26; https://bit.ly/3aNDKC2.) Common contaminated sites include the floor, computer mice, doorknobs, telephones, hand sanitizer dispensers, trash cans, bedrails, bedside tables, remote controls, cell phones, window ledges, patient masks, self-service printers used by outpatients, and health care worker gloves. Viral RNA was identified in the cabins of the Diamond Princess cruise ship up to 17 days after they were vacated (but before cleaning). (MMWR. 2020 Mar 27;69(12):347; https://bit.ly/2xkADUh.) One important caveat to swab studies is that detection of viral RNA is not the same as detection of virus capable of transmitting infection.
The COVID-19 virus persists longer on hard surfaces such as plastic and steel compared with soft surfaces such as cardboard (although it persisted for only four hours on copper). (Lancet Microbe. 2020 Apr 2; https://bit.ly/2KJ82Lk; N Engl J Med. 2020;382:1564; https://bit.ly/2ShCZe4; table 4 online.) These durations represent experimental conditions and may not represent the actual ability to become infected from touching a contaminated surface. Decontamination of objects from outside is still recommended.
Unpublished data from the U.S. Department of Homeland Security Science and Technology Directorate suggest that the coronavirus is inactivated on surfaces in full direct midday sunlight in three minutes and in aerosols in full direct sunlight in 10 minutes. (April 13, 2020. https://bit.ly/2Wad88L; The Washington Post. April 24, 2020; https://wapo.st/2YjnXZ4.)
Fecal Shedding and Bioaerosols
A meta-analysis of 60 studies of 4243 COVID-19 patients found that 17.6 percent had gastrointestinal symptoms, and 48.1 percent of stool samples were positive for viral RNA. (Gastroenterology. 2020 Apr 3; https://bit.ly/2W9Fdxd.) Some patients, particularly children, have had viral RNA detectable in anal swabs longer than respiratory swabs, up to five weeks. (Lancet Gastroenterol Hepatol. 2020;5:434; https://bit.ly/3aQiTxV.)
These findings have raised concerns regarding the possibility of fecal-oral transmission, underscoring the importance of hand hygiene and surface disinfection. A case cluster of women who may have used a common shopping mall restroom (Emerg Infect Dis. 2020 Mar 12;26; https://bit.ly/2YjbjJm) and another that occurred in a men's bathhouse (JAMA Netw Open. 2020 Mar 2;3:e204583; https://bit.ly/2KHLH0Q) with cases transmitted to men who visited one to six days after the index case hint at a fecal vector of transmission.
Fecal viral shedding also increases risks due to toilet bioaerosols. Flushing contaminated toilets aerosolizes large droplets and droplet nuclei that can be carried on air currents, and this continues through multiple flushes. (Am J Infect Control. 2013;41:254; https://bit.ly/2y9wvqw.) Bioaerosols of particles predominantly less than 3 microns in size (the coronavirus is 0.06 to 0.14 microns [StatPearls. 2020 Apr 6; https://bit.ly/2yY9neY]) are aerosolized by toilet flushing and detectable about three feet away and 30 minutes after flushing, even when no waste was present during the flush. (Antimicrob Resist Infect Control. 2018 Jan 26;7:16; https://bit.ly/35eNynm.)
Previous studies have demonstrated enteric and respiratory viruses on 78 percent of hospital and office toilet surfaces (toilet seat, flush handle, door handle) and in 81 percent of toilet-adjacent aerosol samples. (Am J Infect Control. 2014;42:758; https://bit.ly/2W9gzNc.)
Airborne transmission, in the strict definition used by infectious disease experts for varicella, measles, and tuberculosis, is not thought to occur with the coronavirus. A review of 10 studies of the horizontal distance travelled by respiratory droplets found that eight demonstrated a distance farther than six feet, and one showed that exhalations, sneezes, and coughs can create a multiphase turbulent gas cloud that can travel 23-27 feet. (J Infect Dis. 2020 Apr 16; https://bit.ly/3aOvvFJ; JAMA. 2020 Mar 26; https://bit.ly/2SkmHRI.)
Case clusters, including restaurant diners in the path of the air conditioning, choir singers, aircraft travelers, and cruise ship passengers infected after they were confined to their cabins, point toward the possibility of an “airborne-lite” transmission route. The COVID-19 virus was detectable in aerosol for three hours or longer, with a half-life of 1.09 hours. (N Engl J Med. 2020;382:1564; https://bit.ly/2ShCZe4.) Concern has also been raised for carriage of the virus via secondhand smoke generated by smoking and vaping. (Environ Sci Technol. 2020 Apr 22; https://bit.ly/2SlupL7.)
Face masks help by reducing the amount of virus expelled by infected people and providing some filtering of inhaled large respiratory droplets to prevent the virus from reaching the respiratory epithelium. A newly symptomatic man transmitted the virus to five of 39 bus passengers when he wore no mask, but none of 14 after he purchased a mask for the second leg of his journey. (Influenza Other Respir Viruses. 2020 Mar 29; https://bit.ly/2Wato9N.)
Two studies examined various materials that could be used to make homemade masks. (See table 5 online.) Cotton T-shirts and pillowcases were the preferred material.
Incidentally, data show that the highest risk position for a doctor is standing over a COVID-19 patient who is lying on his side and facing the doctor, so examine suspected COVID-19 patients seated or supine, not face-to-face. (Indoor Air. 2018;28:500.)
New data are being reported daily, and this literature synthesis may become rapidly outdated, but table 6 (online) summarizes possible preventive measures for the public and the preventive measures table here (table 7 online) shows those for health care workers.
Dr. Youngis a health sciences clinical professor of pediatrics at the David Geffen School of Medicine at the University of California, Los Angeles, and the director of the pediatric emergency medicine fellowship at Harbor-UCLA Medical Center in Torrance, CA. Follow her on Twitter@kellyyoung16.
An unabridged version of this article is available at https://bit.ly/CornonavirusTransmission with all tables referenced here.