We performed systematic sampling of frequently touched surfaces in the passenger pathways of a major airport during the seasonal influenza epidemic, and detected respiratory virus nucleic acid in 10 % of the samples. We also took a small number of air samples, 25% of which were positive for respiratory virus nucleic acid. Our finding supports the concept of identifying steps in the passenger process for potential transmission of respiratory viruses, and informs planning for preventive measures to reduce secondary spread. This knowledge helps in the recognition of hot spots for contact transmission risk, which could be important during an emerging pandemic threat or severe epidemic.

Our main findings identify that respiratory virus contamination of frequently touched surfaces is not uncommon at airports; and that plastic security screening trays appear commonly contaminated. The latter is consistent with security procedures being an obligatory step for all departing passengers, and that each security tray is rapidly recycled and potentially touched by several hundred passengers per day. Also, that plastic security trays are non-porous and virus survival is known to be prolonged [32, 33].

In a previous study, environmental sampling for respiratory pathogens in Jeddah airport during the 2013 Hajj season revealed presence of viral nucleic acid in 5.5% of air and 17.5% of surface specimens, most commonly from chair handles [22]. The viral pathogens detected in that study included influenza B virus, human adenovirus, and human coronavirus OC43/HKU1. In a different context, a study on virus shedding from patients and environmental deposition of influenza A(H1N1)pdm09 virus, 4.9% of the swabs from surfaces in the immediate vicinity of the patient were positive for viral nucleic acid, and of the samples cultured, 11.7% were positive [17]. Viral nucleic acid was also detected in air samples collected around five of 12 (42%) patients.

The presence of viral RNA of pathogens frequently circulating in the community during the sampling period is not unexpected, as many viruses survive on surfaces for extended periods [32, 34] and viral nucleic acid can be detected for longer than the time for which viability and transmissibility may persist [35]. Influenza A virus has been reported to survive for 24–48 h on non-porous and up to 8–12 h on porous surfaces [32, 33]. For human rhinoviruses, survival times of infective virus and viral RNA have been reported as > 24 h and > 48 h, respectively [20]. Results for survival times for coronavirus on surfaces vary; one investigation found SARS could not be recovered from dried paper, suggesting its survival time was limited [36]. However, findings from other studies indicate survival times for SARS and Middle East respiratory syndrome coronavirus (MERS-CoV) can be much longer, depending on the surface [35]. In a hospital setting in Taiwan, where there was a significant outbreak of SARS, PCR results indicated the presence of SARS on a variety of surfaces suggesting surface contamination should be considered a risk; however no viable virus was cultured [37]. Similarly, in Toronto surface samples in a hospital were positive by PCR for SARS [38]. MERS-CoV has been shown to remain viable on surfaces for longer than influenza A(H1N1) virus [39].

We used a PCR panel employed in our standard respiratory virus surveillance to detect viral nucleic acid in the samples. We did not attempt to recover live viruses by cell culture. Although PCR methodology has limitations because it does not demonstrate the presence of infective virus, it is commonly used to detect the presence of a virus. Also limiting is that the total number of samples taken is relatively small (n = 94). Our sample collection took place within three hours of the daily traffic peaks, well within the reported survival times on surfaces associated with common respiratory viruses. However, whilst the Ct values in our study are similar to those for surface samples in other studies, e.g. [17], these are relatively high, suggesting a low viral load on the surfaces that tested positive, and possibly not constituting the minimum infective dose. Likely due to the high Ct value, subtyping for the influenza A positive specimen was not successful and did not provide information on the origin of the viral strain and its epidemiological context. Alternatively sampling and recovery techniques may have been relatively inefficient, giving an illustration of the potential for transmission, but underestimating the true transmission potential of contaminated surfaces and air. Data concerning the infectious dose specifically for indirect contact are lacking [17]. Killingley and colleagues used a logical argument to conclude that their level of influenza A surface contamination on its own did not represent an infectious dose [17]. The reasoning was that as the copy count in their surface samples approximately only equated to that needed for aerosol transmission, and the likelihood that higher counts are required for indirect transmission, their surface contamination doses would not have been infective. In this study Ct values were similar to Killingley et al. [17], so likewise it is reasonable to conclude that the environmental contamination we identified may not always (or ever) have constituted an infective dose. However, we are unable to determine precisely when each surface became contaminated, and therefore cannot exclude a higher viral load at an earlier time point. Likewise, we cannot establish the efficiency of our sampling technique and the readouts we have may be low due to sampling and recovery techniques. Notwithstanding, we establish the potential for virus transmission from several surfaces. On that basis we do not feel that the potential for transmission can be satisfactorily excluded based on our data.

As previously mentioned, we found the highest frequency of respiratory viruses on plastic trays used in security check areas for depositing hand-carried luggage and personal items. These boxes typically cycle with high frequency to subsequent passengers, and are typically seized with a wide palm surface area and strong grip. Security trays are highly likely to be handled by all embarking passengers at airports; nevertheless the risk of this procedure could be reduced by offering hand sanitization with alcohol handrub before and after security screening, and increasing the frequency of tray disinfection. To our knowledge, security trays are not routinely disinfected. Although this would not eliminate all viruses on hands, (e.g. alcohol gels have been found to be less effective than hand-washing for rhinovirus) [40, 41], it is effective for many viruses, including influenza [42]. In most studies comparing plain soap with alcohol based solutions, the alcohol based solutions were found to be more effective. No respiratory viruses were detected in a considerable number of samples from the surfaces of toilets most commonly touched, which is not unexpected, as passengers may pay particular attention to limiting touch and to hand hygiene, in a washroom environment. Moreover, we did not conduct tests for any enteric viruses.

When an emerging pandemic threat is identified, measures taken to reduce the risk of transmission in an airport, and similar hub environments, could include reducing the risk of indirect transmission, addressing passenger distancing in order to reduce transmission at close proximity (i.e. short range aerosol [43] and droplet transmission), for example in dense queues or at service counters and immigration procedures, enhancing promotion of hand hygiene and respiratory etiquette, and possibly arriving traveler screening procedures. The possible airborne transmission risk can be reduced by ensuring adequate ventilation to dilute pathogen concentrations to sufficiently low levels [44]. Guidelines to mitigate transmission of communicable disease have been issued by Airports Council International [45] and International Civil Aviation Organization [46], but they focus on (exit) screening and handling an individual suspected of having a communicable disease that poses a serious public health risk. A modelling study for entry screening indicated that even in the most optimistic scenarios, the majority of cases of emerging infections would be missed [47]. However, measures preventing transmission locally could be enhanced, for example by improving hand sanitization opportunities where intense, repeat touching of surfaces takes place such as immediately before and after security screening, by enhancing cleaning of frequently touched surfaces, by increased use of non-touch devices, or by effective barriers for face-to-face droplet contact at service counters. Many cleaning agents, household (antibacterial) wipes and anti-viral tissues are able to rapidly render influenza virus nonviable [48], offering multiple simple possibilities and opportunities for reducing the risk of indirect contact transmission.