Study selection
After removal of duplicates, 7439 records were screened for relevance on title and abstract, with 90 reports assessed for eligibility (fig 1). Fifty six additional reports identified from the Comber et al rapid review21 and by citation analysis were also assessed. From these 146 reports, 124 were excluded (see supplementary material 1 (section 3) for list of reasons for exclusion), and 22 reports1323334353637383940414243444546474849505152 relating to 18 studies were included. When two or more reports related to the same study, we considered the most comprehensive report as the main publication.
Flow of articles through the review
All the studies investigated outbreaks of clusters of SARS-CoV-2 infections, and one study had an analytical component.36 Eight studies were conducted in Asia,3435363738394045 five in Europe,4143444748 three in Oceania,323346 and two in the United States.142 Three studies reported on transmission between flats in apartment blocks,383940 two in quarantine hotels,3233 two in restaurants,3435 two in buses,3637 one in a food processing factory,41 one in a courtroom,43 one in an office,44 one in a fitness facility,42 one in a department store,45 and four during singing events.1464748 All the outbreaks occurred in 2020, except for one in January 2021 in South Korea40 (before vaccine rollout started in this country) and one in July 2021 in a quarantine hotel in New Zealand.33
Table 1 and table 2 summarise the studies by setting. Supplementary material 2 provides detailed information on each study.
Summary of included studies, in chronological order by setting: quarantine hotels, restaurants, buses, and apartment blocks
Summary of included studies, in chronological order by setting: department store, singing events, meat processing plant, fitness facility, courtroom, and office
Quality assessment
Figure 2 provides details of the methodological quality ratings: three studies were rated as high quality,333546 five as medium quality,3234364147 and 10 as low quality.1373839404243444548 These ratings represent the methodological quality of descriptive studies.
Quality assessment. *Assessments using quality criteria checklist (QCC) for primary research (see supplementary material 1). †Critical questions: 2 on selection bias, 3 on group comparability, 6 on description of exposure/assessment of transmission routes, and 7 on validity of outcome measurements
Transmission settings
Quarantine hotels
Two outbreaks of covid-19 in quarantine hotels were identified, both in New Zealand and involving cases part of the same genomic cluster who had quarantined in separate rooms. The first outbreak, reported by Eichler et al32 (rated as medium methodological quality) occurred in September 2020, and although primary and secondary cases had travelled on the same flight, transmission is believed to have happened in the hotel on day 12 of quarantine, after the primary case had developed symptoms on day 10. No information was provided on the measures in place at this quarantine hotel (eg, use of face coverings). The second outbreak, reported by Fox-Lewis et al33 (rated as high methodological quality) occurred in July 2021. The primary case (asymptomatic) and secondary cases had travelled on different flights and arrived at the hotel on different days. Staff members, all vaccinated, wore full personal protective equipment and were regularly tested. Participants were asked to wear surgical masks when opening doors, but this could not be validated in the investigation. None of the cases (primary or secondary) were vaccinated; the only person who was vaccinated tested negative despite being part of the same travel group as the secondary cases.
Close contact and fomite transmission were ruled out by video analysis in both studies, although in the outbreak reported by Eichler et al32 fomite transmission through a communal bin—although unlikely, cannot be ruled out. Video analysis showed that in both outbreaks the doors of the rooms had been opened simultaneously for a short period during which infected respiratory particles could have moved between rooms. Both investigations included a review of the ventilation systems and found that pressure differences between rooms and corridors could support this hypothesis. Long distance airborne transmission between a primary case and at least one secondary case was therefore considered to be the most likely route in both outbreaks.
Restaurants
Two separate outbreaks of covid-19 in restaurants were identified. The first outbreak, in China in January 2020, was mainly reported by Li et al34 (rated as medium methodological quality), with additional evidence provided in two other reports.4950 This outbreak involved a primary case (with symptom onset later that day) and at least two secondary cases who were seated on tables between 1.4 and 4.6 m away from the primary case. The second outbreak, reported by Kwon et al35 (rated as high methodological quality), occurred in June 2020 in South Korea and involved three people with confirmed covid-19 who belonged to the same genomic cluster. The primary case, which was presymptomatic at the time, sat 6.5 m from one secondary case for five minutes, and 4.8 m from the other secondary cases for 21 minutes, all at different tables.
After extensive epidemiological and environmental investigations, both studies suggested that the most plausible route was long distance airborne transmission, which could have been facilitated by air circulation units generating a directional air flow from the primary to secondary cases combined with lack of air replacement. In both outbreaks close contact and fomite transmission were ruled out based on video surveillance analysis.
Buses and coaches
Two separate outbreaks of covid-19 on buses in China in January 2020 were identified, one on a journey to and from a worship event among lay Buddhists36 and one on a long distance journey using a public coach and minibus.3751
The outbreak at a worship event was reported by Shen et al36 who conducted a retrospective epidemiological investigation with an analytical component (rated as medium methodological quality). Thirty one of the 300 participants tested positive for SARS-CoV-2 of whom seven were likely to have been infected by close contact transmission during the religious event. The other 23 cases had travelled to the event in the same bus as the primary case and were thought to have been mainly infected during the bus journey, throughout which no one wore face coverings. Those travelling on the bus with the primary case were 11 times more likely to develop covid-19 compared with the other participants (relative risk 11.4, 95% confidence interval 5.1 to 25.4; P<0.01) and 42 times more likely compared with those travelling in the other bus (42.2, 2.6 to 679.3; P<0.01). Close contact transmission, fomite transmission, and transmission from outside the event cannot be ruled out for some of the cases but are unlikely to have accounted for all 23 secondary cases.
The second outbreak, reported by Luo et al37 (rated as low methodological quality) with additional environmental investigations conducted by Ou et al,51 involved one primary case (symptom onset occurred on the day of the event) who had travelled without wearing a face covering on a coach for 2.5 hours with 48 other individuals and then on a minibus for one hour with 12 other individuals. Nine secondary cases were identified, resulting in a secondary attack rate of 15% (95% confidence interval 6% to 24%), with most seated >2 m from the primary case: up to 4.5 m based on one report37 and up to 9.5 m based on the other report.51 Genomic sequencing was not performed and, based on symptom onset dates, it is plausible that more than one primary case was present, reducing our confidence in the distances reported. However, even taking into account all potential primary cases, it is possible that airborne transmission occurred for some secondary cases seated >2 m from a primary case. Some passengers wore face coverings, but none of the secondary cases did.
In both outbreaks, insufficient air replacement and directional airflow from the heating system were hypothesised as promoting long distance airborne transmission, supported by tracer gas experiments in the buses involved in one of the outbreaks.51
Apartment blocks
Three outbreaks of covid-19 in three separate residential apartment blocks were identified. The study by Lin et al38 (rated as low methodological quality) investigated an outbreak involving nine people who tested positive for SARS-CoV-2 in three flats of a 29 storey apartment block in China. The nine cases, identified between 27 January and 13 February 2020, lived in flats that shared drain and sewer pipes connected via an exhaust pipe to the roof. Except for cases in the same household, close contact and fomite transmission were ruled out based on interviews with the cases and partial video analysis (lift only). Some but not all of the cases reported wearing face coverings in the communal areas of the building.
The two other outbreaks were in South Korea. The first, reported by Hwang et al39 (rated as low methodological quality), occurred in August 2020 in an apartment block of 267 flats and involved 10 cases from seven households located around two ventilation ducts (eight cases around one, two around another). The second outbreak, reported by Han et al40 (rated as low methodological quality), occurred in January 2021 in a complex of 260 flats, in which cases located in three flats along the same drainpipe and ventilation duct could not be explained by close contact or fomite transmission. For both outbreaks, transmission routes were mainly investigated through interviews with cases, and therefore recall bias (no video analysis) was possible. All cases reported wearing face coverings in the communal areas of the buildings.
For all three outbreaks, long distance airborne transmission between flats through vertical air ducts or floor drains was deemed possible for at least some of the secondary cases, although environmental investigation (tracer gas experiment) to support this hypothesis was conducted in only one38 of the three studies. In two of the three studies,3840 the ventilation ducts were found to be malfunctioning, which could have contributed to transmission risk. However, only one of these studies39 tested all residents and only one conducted whole genome sequencing,40 which reduces confidence in the results.
Other indoor settings
The other outbreaks identified in this review occurred in a food processing factory,41 fitness facility,42 courtroom,43 office,44 and department store.45
Gunther et al41 (rated as medium methodological quality) reported on an outbreak in a meat processing plant in Germany in May and June 2020 in which 31 out of the 140 workers on the same shift had tested positive for SARS-CoV-2 and were part of the same genomic cluster. Although close contact or fomite transmission in other areas of the processing plant and outside the factory (some workers shared accommodation and carpools) was possible for some cases, the spatial distribution of the cases suggested that transmission was likely to have occurred on the processing line at distances up to 12 m from the primary case who was asymptomatic. The authors hypothesised that factors such as increased respiratory rates (from physically demanding work), lack of air replacement, and continuous recirculation of cooled unfiltered air might have promoted long distance airborne transmission, but these were not investigated further. Some covid-19 measures were in place, including increased distance between workers and use of single layer face coverings, but adherence was not assessed as part of the study.
Groves et al42 (rated as low methodological quality) reported on an outbreak involving two fitness instructors at classes taught in three different facilities in June and July 2020, although the investigation suggested that close contact and fomite transmission were likely to have occurred in all classes but one. The class in which long distance airborne transmission might have happened was a one hour static cycling class in which bikes were placed at least 1.8 m apart, with doors and windows closed and three large fans directed towards the class participants. The instructor, who had shouted instructions while facing the participants, was identified as being the primary case (with symptom onset the next day) and all 10 class participants had tested positive for SARS-CoV-2 three to six days after the class. Face coverings had not been used during the class.
In an outbreak in a courtroom in Switzerland reported by Vernez et al43 (study rated as low methodological quality), five out of the 10 participants at a three hour hearing held on the 30 September 2020 tested positive for SARS-CoV-2. The use of face coverings was mandatory in the building, but not when seated, and social distancing measures were in place, with a minimum of 1.5 m between each seat. Long distance airborne transmission (1.5-3 m) was likely to have happened between a primary case (with symptom onset on that day) and three secondary cases, although close contact or fomite transmission after the hearing or in the bathroom cannot be ruled out. The hypothesis that a lack of air replacement (doors and windows were closed and there was no mechanical ventilation) might have promoted long distance airborne transmission was supported by field measurements and modelling.
Sarti et al44 (rated as low methodological quality) reported on an outbreak in an office in Italy in which five of six coworkers were identified as cases. One of the five coworkers was identified as the primary case, and transmission happened before symptom onset. The sixth coworker, who was not infected, was not present in the office for the two days before symptom onset of the primary case. This transmission event happened in November and December 2020 when mitigation measures were in place, including social distancing, acrylic panels between desks, hand hygiene, and use of a face covering except when seated at a desk. The office was not well ventilated (no air conditioning and windows were closed), which could have promoted long distance airborne transmission. On the basis of the investigation, however, close contact, fomite transmission, and transmission from outside the event cannot be ruled out, so it is unclear as to whether long distance airborne transmission was the most likely route.
Jiang et al45 (rated as low methodological quality) reported on an outbreak linked to a department store that occurred in January 2020 in Tianjin, China, involving 24 cases (six staff and 18 customers). Airborne transmission was considered as the most likely route of transmission between a primary case and 12 secondary cases, which might have been promoted by a lack of air replacement (doors were closed) and high density of people in the store. As genomic sequencing of SARS-CoV-2 was not performed, however, transmission from outside this event cannot be ruled out and, based on symptom onset dates, it is possible that several primary cases were present. On the basis of this investigation, it is unclear whether long distance airborne transmission had occurred in the store.
Singing events
In addition to transmission events associated with specific settings, four epidemiological investigations reporting on outbreaks linked to singing events were identified.
Katelaris et al46 (rated as high methodological quality) reported on an outbreak in Sydney, Australia, linked to a series of four church services held between 15 and 17 July 2020. The probable primary case, a choir member, had sung at each of these one hour services, and 12 secondary cases were identified (2.4% secondary attack rate across the four services), who had sat in the same section of the church, between 1 m and 15 m from the primary case. Viral genomic sequencing of the primary case and 10 secondary cases showed a single genomic cluster, suggesting that transmission had occurred during the church services.
The second epidemiological investigation47 (rated as medium methodological quality; preprint) reported on five singing events held between September and October 2020 in the Netherlands. At the time, national recommendations were in place to reduce covid-19 transmission, and although singing in groups was allowed, physical distancing (>1.5 m) and ventilation were recommended. Each singing event had between nine and 21 attendees, and attack rates of between 53% and 74% were observed. Fomite transmission was deemed unlikely in all but one event, but close contact transmission was considered possible for some of the secondary cases in three of the five events. However, owing to the high secondary attack rates, it is possible that at least some of the secondary cases had been infected via long distance airborne transmission and, even though ventilation through open doors or windows was reported for all events, air exchange rates were likely to have been low in at least three of the five events.
The two other outbreaks occurred in March 2020—that is, during the early stage of the pandemic when no mitigation measures were in place. One of them (70% attack rate, including probable cases) happened in France during a two hour choral rehearsal in a narrow, indoor, non-ventilated space48 (study rated as low methodological quality). The second outbreak (87% secondary attack rate, including probable cases) after a 2.5 hour choral rehearsal on 10 March 2020 in Washington (USA) was initially reported by Hamner et al1 (rated as low methodological quality) and further discussed by Miller et al.52 For both outbreaks, close contact and fomite transmission were only assessed through interviews and cannot be fully ruled out. The high secondary attack rate, however, suggests that long distance airborne transmission might have occurred for at least some of the cases.
The results from the four studies suggest that long distance airborne transmission was likely to have occurred for at least some of the transmission events, and that singing may have increased the amount of aerosol generated by the primary cases, which is consistent with modelling results reported by some of these authors.5253
Summary and critical analysis of results
Seven of the outbreaks identified1343637384548 occurred in the early stage of the pandemic (January-March 2020) when knowledge of covid-19 was limited, especially the incubation period and the extent of asymptomatic or presymptomatic transmission. As a result, most of these studies only conducted symptomatic testing and considered potential secondary cases to be participants with symptom onset soon after the potential exposure event, including the next day. In addition, for the studies conducted in January 2020 in China and in March 2020 in Europe or the US, it is possible that community transmission was higher than perceived at the time.
Therefore, in an outbreak such as the one reported by Luo et al37 where no genomic sequencing was conducted and three of the nine secondary cases developed symptoms or tested positive for SARS-CoV-2 one or two days after exposure, it is plausible that more than one primary case was present and that transmission occurred through means other than long distance airborne transmission. In two of the studies reporting on singing events,148 genomic sequencing and asymptomatic testing were not carried out and some of the secondary cases developed symptoms in the days after exposure but because of the high attack rates reported for these outbreaks, it is possible that long distance airborne transmission had happened for at least some of the transmission events. Long distance airborne transmission was also considered possible for two other early studies as a result of detailed epidemiological investigations.3436 However, the plausibility of long distance airborne transmission for the outbreak in the department store was unclear as other transmission routes could not be ruled out.45
Among the other studies, four33354146 provided convincing evidence for long distance airborne transmission as a result of detailed epidemiological investigations combined with genomic sequencing. Eichler et al32 also conducted genomic sequencing but their reporting of the epidemiological investigation was not sufficiently exhaustive to exclude other transmission routes (close contact or fomite) for the only secondary cases who could have been infected by long distance airborne transmission. The investigations by Shah et al,47 Hwang et al,39 Groves et al,42 Han et al,40 and Vernez et al43 suggested that long distance airborne transmission was possible for at least some of the transmission events (close contact or fomite could not be fully ruled out), but stronger conclusions could not be drawn owing to methodological limitations (including the absence of genomic sequencing and risk of selection bias). Finally, the likelihood of long distance airborne transmission was unclear in the outbreak in the office reported by Sarti et al44 as, despite the covid-19 measures in place, close contact and fomite transmission could not be completely ruled out on the basis of the investigation.
Eleven of the 18 studies reported on the use of face coverings.3335363738394041424344 Overall, the information provided was limited, and two of these studies only mentioned that face coverings were compulsory in the settings of interest (quarantine hotel33 and food processing factory41) without reporting on adherence or behaviour (eg, whether workers wore face coverings correctly for the duration of their shift). Based on this limited information, we found no evidence of long distance airborne transmission where participants were known to have worn face coverings for the duration of exposure.
Only one of the outbreaks33 identified occurred at a time when covid-19 vaccines were available, although in this outbreak the primary and secondary cases were not vaccinated.
Grading of the evidence
Table 3 provides the grading of the evidence for each of the primary outcomes: SARS-CoV-2 infection via airborne transmission at a distance >2 m, insufficient air replacement (modifying factor), directional air flow (modifying factor), and increased aerosol emission when singing, speaking loudly, or doing intense physical work (modifying factor). Assessment of modifying factors was considered not applicable for the two outbreaks where the likelihood of long distance airborne transmission had been judged as unclear.
Summary of findings using Grading of Recommendations, Assessment, Development, and Evaluation approach
For all four outcomes, the evidence was judged as having methodological limitations owing to study design and to be at serious risk of imprecision owing to small numbers of participants as well as some risk of bias in exposure or outcome assessment, or both. However, the risks of inconsistency and indirectness were judged as not serious as the results were consistent across studies conducted in a range of settings and with different populations and provide evidence of direct relevance to the public health question of interest. The risk of publication bias was judged to be serious for the outcome of SARS-CoV-2 infection through airborne transmission at a distance >2 m and for the modifying factor of activities associated with increased emission of aerosols, but not serious for the modifying factors of insufficient air replacement and directional air flow. As a result, the certainty of evidence was judged as very low for all outcomes.
Because of high heterogeneity between studies, the additional outcomes of time spent in the transmission setting and distance over which airborne transmission was thought to have occurred could not be summarised or graded using the GRADE framework. Exposure timings ranged from five minutes to three hours, and distances were up to 15 m.
link