Advertisement

Probable close contact transmission in a restaurant in China

Published:August 30, 2022DOI:https://doi.org/10.1016/j.jinf.2022.08.029

      Highlights

      • Real human behaviors on close contact and surface touch was used to analyze the dominant route of SARS-CoV-2 transmission in the restaurant.
      • Close contact route may dominate the outbreak of B.1.617.2 (Delta) variant in the restaurant.
      • Fomite was not the main transmission route in this particular restaurant outbreak.
      • Virus exposure via close contact route was hundreds times higher than it via long-range airborne route.
      • Virus exposure risk of diners who sit next to the infected had an exposure risk over 1000 times higher than that of staff.
      Dear Editor
      Recently, we published a study
      • Zhang N.
      • Chen X.
      • Jia W.
      • Jin T.
      • Xiao S.
      • Chen W.
      • et al.
      Evidence for lack of transmission by close contact and surface touch in a restaurant outbreak of COVID-19.
      regarding the probable long-range airborne transmission in a restaurant in China by filtering out both close contact and fomite routes. In this specific context, we found that close contact transmission may predominate a COVID-19 outbreak caused by the B.1.617.2 (Delta) variant in a China's restaurant via 133,446 human behavior data points relevant to virus transmission (surface touching and close contacts) from analysis of video recordings.
      Restaurants are a high-risk indoor environment for SARS-CoV-2 transmission, due to frequent close contact, crowding and masking impossibility.
      • Lu J.
      • Gu J.
      • Li K.
      • Xu C.
      • Su W.
      • Lai Z.
      • et al.
      COVID-19 outbreak associated with air conditioning in restaurant, Guangzhou, China, 2020.
      ,
      • Pray I.W.
      • Kocharian A.
      • Mason J.
      • Westergaard R.
      • Meiman J.
      Trends in outbreak-associated cases of COVID-19—Wisconsin, March–November 2020.
      However, it is difficult to identify whether it was close contact or fomite transmission that dominated COVID-19 outbreaks in restaurants, due to a lack of data of indoor human behavior.
      A COVID-19 outbreak caused by the B.1.617.2 (Delta) variant in a restaurant in Guangzhou on May 23, 2021 resulted in 10 diners being infected (Fig. 1, Appendix A). Human behaviors on close contact and surface touching were collected by video recordings during the lunch time (Appendix B). Combining the data on human behaviors and established indoor transmission model (Appendix C), the virus exposure via close contact, fomite, and long-range airborne route of all diners and staff was estimated.
      Fig 1
      Fig. 1Setting of the restaurant. (A) Floor plan; (B) image obtained from the video camera.
      According to the epidemiological investigation of the outbreak and the gene sequencing results, D4 was the most likely infectious source for the outbreak. However, since D20 may be an infectious source, we considered a total of 15 scenarios (Appendix D).
      A total of 3108 close contacts with the total duration of 29,362 s were identified (Appendix E). D12 and D13 were involved in the most close-contacts (110), while D26 and D27 had the longest close contact duration of 2340s. Focusing on the possible source infectors (D4 and D20), we noted no close contact between them and diners sitting at Tables 4 and 5, and no diners sitting at Tables 4 and 5 were infected. D4 had a close contact of only 41 s with S1, no other close contacts between D4/D20 and staff were identified (Fig. 2A). Close contact was likely to be the dominant virus transmission route in the restaurant when only D4 or both D4 and D20 were the infectious source (with p <0.01 or <0.05). D20 was not the only source of infection in the restaurant outbreak. If D4 was the source, D3 would have had the highest virus exposure via both short-range inhalation and mucous deposition during the lunch, but D3 did not get infected. If D20 was the only source, only D21 would have been exposed to the virus via the close contact route, which was also an impossibility. If D4 or both D4 and D20 were the sources, D18 would have had the lowest exposure via both short-range inhalation (0.35% of exposure of D4) and mucous deposition (0.30% of exposure of D4).
      Fig 2
      Fig. 2Virus transmission potential via close contact and fomite routes. (A) total duration between possible source infectors (D4 and D20) and other diners and staff; (B) Virus transmission via the fomite route for different source infectors.
      A total of 14,687 touches with a total duration of 206,334 s were identified (Appendix F). Diners and staff on average spent 84.4% (91.5%) and 78.9% (85.6%) of their indoor time touching surfaces with their left (right) hand. The simulation results for virus intake fraction via the fomite route for different source infectors is shown in Fig. 2B. Only one out of five staff (S4) had any fomite route virus exposure, because the other four staff members did not touch their mucosa during the lunch period. Infected diner, D18 never touched her mucosa during the lunch period either. We found that the average intake fraction by infected people was only 80.5% (30.8% - 154.4%) higher than it of susceptible people, and that there was no significant difference in virus exposure between the susceptible and the infected for all scenarios.
      With an indoor ventilation rate of more than 5 ACH (6 L/s per person), the indoor virus concentration was no more than 1400/m3. Compared with exposure via short-range inhalation, long-range inhalation contributed relatively little (0.3%) (Appendix G). The fomite route was not the main transmission route in this outbreak, but that close contact may be. D4 or both D4 and D20 were the most likely source infectors of this outbreak.
      It is believed that close contacts, which include short-range airborne, are a high risk transmission route.
      • Zhang N.
      • Liu X.
      • Jin T.
      • Zhao P.
      • Miao D.
      • Lei H.
      • et al.
      Weakening personal protective behavior by Chinese university students after COVID-19 vaccination.
      ,
      • Zhang N.
      • Lei H.
      • Li L.
      • Jin T.
      • Liu X.
      • Miao D.
      • et al.
      COVID-19 vaccination did not change the personal protective behaviors of healthcare workers in China.
      Restaurants may have an extremely high rate of SARS-CoV-2 exposure via the close contact route because of high close contact rate (20%) without masks.
      • Zhang N.
      • Chen X.
      • Jia W.
      • Jin T.
      • Xiao S.
      • Chen W.
      • et al.
      Evidence for lack of transmission by close contact and surface touch in a restaurant outbreak of COVID-19.
      In offices, people spend around 10% of their time in close contact.
      • Zhang N.
      • Su B.
      • Chan P.T.
      • Miao T.
      • Wang P.
      • Li Y.
      Infection spread and high-resolution detection of close contact behaviors.
      To quickly track close contacts in crowded and poorly ventilated indoor environments such as a restaurant, QR codes (location codes), which are unique to each public place, can be used. After people scan the location code with a mobile device, an electronic record including basic information such as arrival and departure times, would be generated for a specific indoor environment. This information could be used solely for public health responses. On the other hand, previous studies
      • Kang M.
      • Yi Y.
      • Li Y.
      • Sun L.
      • Deng A.
      • Hu T.
      • et al.
      Effectiveness of inactivated COVID-19 vaccines against illness caused by the B.1.617.2 (Delta) variant during an outbreak in Guangdong, China: a cohort study.
      have shown that vaccination is effective in COVID-19 prevention and control. To reduce exposure via the close contact route in restaurants, some cities implemented strategies such as limiting the number of diners (e.g. restaurant cannot fill more than 50% of its capacity), tables were required to be at least 1.5 m apart,
      • Zhang N.
      • Jia W.
      • Lei H.
      • Wang P.
      • Zhao P.
      • Guo Y.
      • et al.
      Effects of human behaviour changes during the COVID-19 pandemic on influenza spread in Hong Kong.
      and dividers to be put on tables to separate diners.
      • Liu Z.
      • Li R.
      • Wu Y.
      • Ju R.
      • Gao N.
      Numerical study on the effect of diner divider on the airborne transmission of diseases in canteens.
      In general, this study showed that close contact was the main transmission route of the outbreak (B.1.617.2 (Delta) variant) in the restaurant, although a previous study
      • Zhang N.
      • Chen X.
      • Jia W.
      • Jin T.
      • Xiao S.
      • Chen W.
      • et al.
      Evidence for lack of transmission by close contact and surface touch in a restaurant outbreak of COVID-19.
      ,
      • Li Y.
      • Qian H.
      • Hang J.
      • et al.
      Probable airborne transmission of SARS-CoV-2 in a poorly ventilated restaurant.
      showed that long-range airborne route dominated the outbreak (initial strain: NC_045512) in another restaurant. This may be explained in the difference in ventilation. the indoor ventilation in the previous outbreak was very poor, at 0.9 L/s per person.
      • Li Y.
      • Qian H.
      • Hang J.
      • et al.
      Probable airborne transmission of SARS-CoV-2 in a poorly ventilated restaurant.
      In this newly studied outbreak the ventilation is much better in the restaurant. The restaurant has large doors, which were open. Obviously, involved variants of SARS-CoV-2 are different in the two outbreaks. One would expect some differences in the main transmission route, but there is no supporting evidence.

      Declaration of Competing Interest

      The authors declare that they have no competing interests.

      Acknowledgements

      This work was supported by the National Natural Science Foundation of China (grant numbers: 52108067 ); the Key-Area Research and Development Program of Guangdong Province ( 2019B111103001 ).

      Appendix. Supplementary materials

      Reference

        • Zhang N.
        • Chen X.
        • Jia W.
        • Jin T.
        • Xiao S.
        • Chen W.
        • et al.
        Evidence for lack of transmission by close contact and surface touch in a restaurant outbreak of COVID-19.
        J Infect. 2021; 83: 207-216
        • Lu J.
        • Gu J.
        • Li K.
        • Xu C.
        • Su W.
        • Lai Z.
        • et al.
        COVID-19 outbreak associated with air conditioning in restaurant, Guangzhou, China, 2020.
        Emerg Infect Dis. 2020; 26: 1628-1631
        • Pray I.W.
        • Kocharian A.
        • Mason J.
        • Westergaard R.
        • Meiman J.
        Trends in outbreak-associated cases of COVID-19—Wisconsin, March–November 2020.
        Morb Mort Wkly Rep. 2021; 70: 114-117
        • Zhang N.
        • Liu X.
        • Jin T.
        • Zhao P.
        • Miao D.
        • Lei H.
        • et al.
        Weakening personal protective behavior by Chinese university students after COVID-19 vaccination.
        Build Environ. 2021; 206108367
        • Zhang N.
        • Lei H.
        • Li L.
        • Jin T.
        • Liu X.
        • Miao D.
        • et al.
        COVID-19 vaccination did not change the personal protective behaviors of healthcare workers in China.
        Front Public Health. 2021; 9777426
        • Zhang N.
        • Su B.
        • Chan P.T.
        • Miao T.
        • Wang P.
        • Li Y.
        Infection spread and high-resolution detection of close contact behaviors.
        Int J Environ Res Public Health. 2020; 17: 1445
        • Kang M.
        • Yi Y.
        • Li Y.
        • Sun L.
        • Deng A.
        • Hu T.
        • et al.
        Effectiveness of inactivated COVID-19 vaccines against illness caused by the B.1.617.2 (Delta) variant during an outbreak in Guangdong, China: a cohort study.
        Ann Intern Med. 2022; 175: 533-540
        • Zhang N.
        • Jia W.
        • Lei H.
        • Wang P.
        • Zhao P.
        • Guo Y.
        • et al.
        Effects of human behaviour changes during the COVID-19 pandemic on influenza spread in Hong Kong.
        Clin Infect Dis. 2021; 73: e1142-e1150
        • Liu Z.
        • Li R.
        • Wu Y.
        • Ju R.
        • Gao N.
        Numerical study on the effect of diner divider on the airborne transmission of diseases in canteens.
        Energ Build. 2021; 248111171
        • Li Y.
        • Qian H.
        • Hang J.
        • et al.
        Probable airborne transmission of SARS-CoV-2 in a poorly ventilated restaurant.
        Build Environ. 2021; 196107788