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Transmissibility and Transmission of Respiratory Viruses

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Transmissibility and Transmission of Respiratory Viruses REVIEWS Transmissibility and transmission of respiratory viruses Nancy H. L. Leung Abstract | Human respiratory virus infections lead to a spectrum of respiratory symptoms and disease severity, contributing to substantial morbidity, mortality and economic losses worldwide, as seen in the COVID-19 pandemic. Belonging to diverse families, respiratory viruses differ in how easy they spread (transmissibility) and the mechanism (modes) of transmission. Transmissibility as estimated by the basic reproduction number (R0) or secondary attack rate is heterogeneous for the same virus. Respiratory viruses can be transmitted via four major modes of transmission: direct (physical) contact, indirect contact (fomite), (large) droplets and (fine) aerosols. We know little about the relative contribution of each mode to the transmission of a particular virus in different settings, and how its variation affects transmissibility and transmission dynamics. Discussion on the particle size threshold between droplets and aerosols and the importance of aerosol transmission for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and influenza virus is ongoing. Mechanistic evidence supports the efficacies of non-pharmaceutical interventions with regard to virus reduction; however, more data are needed on their effectiveness in reducing transmission. Understanding the relative contribution of different modes to transmission is crucial to inform the effectiveness of non-pharmaceutical interventions in the population. Intervening against multiple modes of transmission should be more effective than acting on a single mode. Human respiratory viruses include a broad range of supporting different modes of transmission will aid in viruses that infect cells of the respiratory tract, elicit the control of respiratory virus transmission. respiratory and other symptoms, and are transmitted Previous reviews and commentaries discussed the mainly by respiratory secretions of infected persons. transmissibility of influenza virus4,5; methods for stud- Respiratory virus infections often cannot be differen- ying transmission, including animal models4–7, human tiated clinically. Respiratory viruses belong to diverse models6,8 and epidemiological studies9; the mechanism virus families that differ in viral and genomic structures, and evidence for different modes of transmission4,6,7,9–12; populations susceptible to infection, disease severity, factors affecting transmission4,5,11,13; controversies seasonality of circulation, transmissibility and modes regarding the relative importance of different modes of transmission. Together, they contribute to substantial of transmission14,15; pharmaceutical interventions4 and morbidity1, mortality2 and concomitant economic losses3 NPIs11,16–18 for mitigating transmission16–19; and guide- annually worldwide. In addition, occasional pandemics lines from public health agencies on infection pre- cause extreme disruption to societies and economies as vention and control recommendations for respiratory exemplified by the current COVID-19 pandemic. Until viruses9,15. These various aspects of transmissibility and effective treatments or vaccines for COVID-19 are transmission have been more comprehensively studied 4–7,10,14,17,19 WHO Collaborating Centre available, we have to rely heavily on population- based for influenza virus than for other respiratory 9,11,12,15,16,18 for Infectious Disease and individual- based public health measures to miti- viruses . In this Review, I will bring these dis- Epidemiology and Control, gate transmission. The effectiveness and the suitability cussions together to provide a broad overview of the School of Public Health, Li Ka of a non- pharmaceutical intervention (NPI) to mit- transmissibility and modes of transmission of respira- Shing Faculty of Medicine, igate transmission depends substantially on the ease tory viruses, the approaches used to make these assess- The University of Hong Kong, Hong Kong Special of trans mission (transmissibility) and the mechanism of ments, the viral, host and environmental determinants Administrative Region, China. transmission (modes of transmission) specific to that of transmission, and common NPIs for mitigating e- mail: [email protected] virus, as these interventions can target some but not all respiratory virus transmission, in the hope of illustrat- https://doi.org/10.1038/ potential modes of transmission. Therefore, understand- ing the common approaches for studying respiratory s41579-021-00535-6 ing how to evaluate the transmissibility and evidence virus transmission as well as the interconnection and 528 | AUGUST 2021 | VOLUME 19 www.nature.com/nrmicro 0123456789();: REVIEWS differences between these discussions. I also discuss to evaluate the molecular determinants of transmissi- recent controversies regarding the role of aerosols in bility20, the airborne transmission potential of emerg- transmission of severe acute respiratory syndrome ing viruses21 or drug- resistant viruses22, the relative coronavirus 2 (SARS- CoV-2), and the difficulties in importance of droplets and aerosols to transmission23 evaluating the relative contribution of each mode to the and the anatomical site that drives the different routes transmission of respiratory viruses. of transmission24. Alternatively, volunteer transmission studies, where transmission is observed in susceptible Transmissibility volunteers who are exposed to other volunteers who are In the control of a novel pandemic, one of the most either experimentally or naturally infected8, may be used important early questions is how easily the disease will to provide important information on the effectiveness spread from an infected person to a susceptible person; of interventions and the importance of presymptomatic that is, how transmissible the disease is. Transmissibility or asymptomatic transmission in a controlled setting25. is determined by the infectivity of the pathogen, the con- However, these studies can be challenging and expensive tagiousness of the infected individual, the susceptibility to conduct, and may be criticized as too artificial8. of the exposed individual, the contact patterns between the infected individual and the exposed individual, Evaluating transmissibility in the population and the environmental stress exerted on the pathogen Mathematical or statistical models are often used to esti- during transmission. These will determine the scale mate transmissibility of a respiratory virus in the popula- and intensity of control measures needed to suppress tion, especially during pandemics to assess the extent of transmission. In animal models, volunteer transmis- transmission. With use of data from surveillance, obser- sion studies, modelling studies and observational as vational and interventional epidemiological studies, or well as interventional epidemiological studies, although simulation from modelling studies, transmissibility is the number of successful transmission events (that is, usually assessed by the estimation of the basic reproduc- (BOx 2) infection in the exposed individual) is often used as an tion number (R0) or secondary attack rate (SAR) . outcome measure, these study designs answer different In addition, by comparing the two simultaneously, one research questions when evaluating the transmissibility can assess the role of specific populations (for example, of a respiratory virus. households or schools)26 or superspreading events27 in driving community transmission. Evaluating transmissibility in animals and volunteers Animal models are often used to compare the transmis- Modes of transmission sibility of respiratory viruses with different naturally Respiratory viruses are transmitted between individuals occurring or engineered genomic constructs to identify when the virus is released from the respiratory tract of viral molecular determinants of increased transmissibil- an infected person and is transferred through the envi- ity, or to compare the transmissibility between different ronment, leading to infection of the respiratory tract of modes of transmission (BOx 1) . For example, for influ- an exposed and susceptible person. There are a number enza virus, animal transmission studies have been used of different routes (or modes) through which transmis- sion could occur, the chance of which is modified by Box 1 | Evaluating transmissibility in animal transmission studies viral, host and environmental factors. Although there is evidence in support of individual modes of transmission, In the simplest form of animal transmission studies, naive (‘infector’ or ‘donor’) animals the relative contribution of different modes to a success- are first inoculated with a candidate virus, with infection confirmed by the recovery ful transmission event, and the relative effect of each of virus in respiratory specimens; other naive (‘infectee’ or ‘contact’) animals are then co- housed with the infected animals for some period to observe whether the contact factor on each mode or multiple modes simultaneously, animal subsequently acquires infection. The number of donor and contact animals used is often unknown. may vary, or multiple donor–contact pairs of animals are used, and transmissibility is assessed by counting the proportion of contact animals infected204. This basic design Direct contact, indirect contact, droplet and aerosol can be adjusted to study transmissibility for different modes of transmission: direct Respiratory viruses can be transmitted via respiratory contact transmission
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