R E S E A R C H A R T I C L E Open Access
Deposition of respiratory virus pathogens
on frequently touched surfaces at airports
, Carita Savolainen-Kopra
, Joanne E. Enstone
, Ilpo Kulmala
, Pertti Pasanen
, Anniina Salmela
, Jonathan S. Nguyen-Van-Tam
, Petri Ruutu
and for the PANDHUB consortium
Background: International and national travelling has made the rapid spread of infectious diseases possible. Little
information is available on the role of major traffic hubs, such as airports, in the transmission of respiratory infections,
including seasonal influenza and a pandemic threat. We investigated the presence of respiratory viruses in the passenger
environment of a major airport in order to identify risk points and guide measures to minimize transmission.
Methods: Surface and air samples were collected weekly at three different time points during the peak period
of seasonal influenza in 2015–16 in Finland. Swabs from surface samples, and air samples were tested by real-
time PCR for influenza A and B viruses, respiratory syncytial virus, adenovirus, rhinovirus and coronaviruses
(229E, HKU1, NL63 and OC43).
Results: Nucleic acid of at least one respiratory virus was detected in 9 out of 90 (10%) surface samples,
including: a plastic toy dog in the children’s playground (2/3 swabs, 67%); hand-carried luggage trays at the
security check area (4/8, 50%); the buttons of the payment terminal at the pharmacy (1/2, 50%); the handrails
of stairs (1/7, 14%); and the passenger side desk and divider glass at a passport control point (1/3, 33%).
Among the 10 respiratory virus findings at various sites, the viruses identified were: rhinovirus (4/10, 40%,
from surfaces); coronavirus (3/10, 30%, from surfaces); adenovirus (2/10, 20%, 1 air sample, 1 surface sample);
influenza A (1/10, 10%, surface sample).
Conclusions: Detection of pathogen viral nucleic acids indicates respiratory viral surface contamination at
multiple sites associated with high touch rates, and suggests a potential risk in the identified airport sites. Of
the surfaces tested, plastic security screening trays appeared to pose the highest potential risk, and handling
these is almost inevitable for all embarking passengers.
Keywords: Influenza virus, Respiratory virus, Surface contamination, Airport
The continuous growth in air travel  increases the
likelihood of rapid spread of infectious diseases between
countries and continents. Air travel made possible the
rapid spread of Severe Acute Respiratory Syndrome
(SARS) from Hong Kong in 2003 to several countries in
a very short time , as was the case for the global
spread of pandemic influenza A(H1N1)pdm09 from
Mexico and the United States of America in 2009 .
Symptomatic and asymptomatic respiratory tract in-
fections are common among passengers , with poten-
tial for transmission to fellow passengers during
pre-embarkation and travel, or after arrival at destin-
ation, via multiple modes of transmission, including air-
borne, droplet and contact transmission. Transmission
of a range of infections during air travel has been inves-
tigated and recommendations for control and incident
investigation have been published [5–9]. Confirmed in-
fluenza transmission has also been reported aboard ships
, and transmission of influenza-like illness has been
reported aboard ships  and trains . The potential
for airports to spread an infection causing pandemic
threat globally has been modelled estimating how
* Correspondence: firstname.lastname@example.org
Department of Health Security, National Institute for Health and Welfare,
P.O.Box 30, 00271 Helsinki, Finland
Full list of author information is available at the end of the article
© The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Ikonen et al. BMC Infectious Diseases (2018) 18:437
individual airports could contribute to an epidemic
Major traffic hubs, particularly large airports receive
passengers from multiple continents [14,15]. There is
little published literature on the role of airports or other
major hubs (e.g. ports and railway stations) in the trans-
mission of infections, or on the main risk points within
a hub for transmission. One published event involved a
patient travelling through an airport with measles (which
transmits efficiently through air in closed premises),
where epidemiological investigation showed transmis-
sion to other passengers in the airport .
Virus sampling of the touched environment has been
previously performed in many settings, including for ex-
ample, hospitals, homes of patients infected with influ-
enza [17,18], children’s nurseries , homes of people
infected with rhinovirus  and a hotel setting . To
our knowledge, only one such study has been published
pertaining to an airport environment, which found that
out of 40 surfaces tested, 17.5% were positive for at least
one of a number of viral pathogens, including influenza.
. We have supplemented these findings by investigat-
ing the presence of respiratory viruses in the passenger
environment of an airport in order to identify risk points
and guide measures to minimize transmission.
Study site and sampling
Helsinki-Vantaa airport is the main airport in Finland,
with a throughput of 18.9 million passengers in 2017.
Approximately 12% of the traffic is to or from Eastern,
South-Eastern and Southern Asia.
The passenger processes within the airport of depart-
ing, transit and arriving passengers were carefully
mapped during an initial site visit, going through the ac-
tual passenger pathway with hub staff, to identify sur-
faces which are frequently touched, and areas where
passenger density would be high (where direct transmis-
sion of respiratory viral pathogens could potentially take
place) (Fig. 1). After a pilot phase in September, 2015, to
test sampling procedures, sampling for the study was
performed in February 2016 at the peak period of the
2015–16 annual influenza epidemic in Finland .
Surface and air samples were collected weekly at three
different time points (weeks 5–7/2016: 4.2.2016–
17.2.2016) from a variety of sites along the passenger
Fig. 1 Passenger processes in the Helsinki –Vantaa Airport
Ikonen et al. BMC Infectious Diseases (2018) 18:437 Page 2 of 7
flow pathways in Helsinki-Vantaa airport (Table 1) from
frequently touched surfaces. The hours of sampling were
immediately after the early morning peak traffic (0700-
0900 h), after the noon peak (1100-1200 h), and after
the mid-afternoon peak hours (1400 h –1600 h), during
which much of the transit traffic takes place for passen-
gers travelling between Central European and Asian des-
tinations. Sampling time was tailored so that the
surfaces sampled had not been cleaned after the most
recent preceding traffic peak.
The surface samples were taken using nylon swabs,
which were immersed in viral transport medium (VTM)
before sampling. The standard sampling area size was
10 × 10 cm (swab applied in horizontal followed by verti-
cal and diagonal sweeps). For security screening trays at
the security check area, the sample was taken from all
the outer sides of the tray using the same swab, moving
it horizontally, vertically and transversely across the
sampling area, including the area just below the tray’s
lip. For the toilet door knobs and flushing buttons the
swabbing covered the entire touchable surface. The swab
was immediately placed into 1 ml of VTM.
Four air samples were taken during the study period,
two samples at two different times of the day in week 5
and one sample in weeks 6 and 7. The air particles were
collected using an Impactor FH5® sampler (Klotz GmbH,
Germany) with filtration . The sampler was posi-
tioned at approximately 2 m from the floor in the pas-
senger security check area and ran for 33 min. The flow
rate through the sampler was 30 L/min giving a total
sample volume of 1000 L filtered through a gelatin filter
paper (Gelatin Filter Disposables, Sartorius Stedim Bio-
tech GmbH, Germany). Before nucleic acid extraction,
an approximately 0.5 × 5 cm strip of the gelatin filter
paper was immersed and dissolved in 1 ml VTM.
All samples were transported refrigerated and stored
in refrigerator at approximately + 4 °C for short-term
storage (maximum 24 h), and then frozen at approxi-
mately −60 °C for extended storage before nucleic acid
extraction and virus detection.
Nucleic acid extraction and virus detection
Viral nucleic acid was extracted from 100 μl samples
with the Qiagen Qiacube® instrument using RNeasy Mini
Kit® (Qiagen, Hilden, Germany) following the manufac-
turer’s instructions and was eluted in 50 μl. Random
hexamer primers and RevertAid H Minus Reverse Tran-
scriptase (Thermo Fisher Scientific, Massachusetts,
USA) were used in the synthesis of the cDNA. cDNA re-
action was performed at the following conditions:
10 min at 25 °C, 30 min at 42 °C and 10 min at 70 °C.
All samples were tested in three separate multiplex
real-time polymerase chain reaction (real-time PCR)
tests using QuantiTect™Multiplex PCR or NoRox PCR
Kit (Qiagen, Hilden, Germany). Primers and probes for
seasonal influenza A [25–27] (with influenza A(H3)pri-
mer and probe sequences courtesy of Erasmus Medical
Centel, Rotterdam, Netherlands) and B viruses , re-
spiratory syncytial virus , adenovirus , rhinovirus
 and coronavirus (229E, HKU1, NL63 and OC43)
Table 1 Respiratory viruses detected from the surface and air samples
Sample type Sampling area Positive/number of samples Detected respiratory virus
Surface Toilet: upper surface the toilet bowl lid 0/14 none
Surface Toilet: button for flushing 0/14 none
Surface Toilet: lock at the door inside the toilet 0/14 none
Surface Hand-carried luggage boxes at the security check area 4/8 adeno
human corona OC43
Surface Armrest of a chair at the waiting area 0/6 none
Surface Handrails of an escalator 0/10 none
Surface Handrails of stairs 1/7 human corona OC43
Surface Plastic toy dog in children’s playgroung 2/3 rhino
Surface The trolley handles for luggage 0/3 none
Surface The buttons of an elevator 0/3 none
Surface The touch screen on the check-in machine 0/3 none
Surface Desk and divider glass at the passport control point 1/3 rhino
Surface Buttons of payment terminal at the pharmacy 1/2 rhino and human corona OC43
Air At the security check area 1/4 adeno
Ikonen et al. BMC Infectious Diseases (2018) 18:437 Page 3 of 7
 (with probe sequences courtesy of P. Simmonds and
K. Templeton, personal communication) are previously
published. Some modifications have been made in the
probe of influenza A(H1)pdm09 . Primer and probe
sequences for real-time PCR are available on request.
The thermal profile for all three multiplex were 95 °C
for 15 min for enzyme activation followed by 50 cycles
at 95 °C, 55 °C and 45 °C, 45 s in each step using Strata-
gene Mx3005P thermal cycler. The respiratory viruses
selected for this study represent the virus panel that we
use for our standard respiratory virus surveillance.
Altogether, 90 surface samples and four air samples were
collected during weeks 5–7/2016 (Table 1). Nucleic acid
of at least one respiratory virus was detected in 9 surface
samples (10%). Of surface samples from week 5, 6 and 7,
two of 25 (8%), three of 31 (9.7%), and four of 34
(11.8%) respectively were positive.
Viral nucleic acid was found in samples from the sur-
faces of a plastic toy dog in the children’s playground
(two of three swabs, 66.7%), hand-carried luggage trays
at the security check area (four of eight, 50%), the but-
tons of the payment terminal at the pharmacy (one of
two, 50%), the handrails of stairs (one of seven, 14%)
and the passenger side of desk and divider glass at the
passport control points (one of three, 33.3%).
Both rhinovirus and coronavirus OC43 were detected
in the same sample from buttons of the payment ter-
minal at the pharmacy. The samples from the armrest of
chairs at the waiting area (6 samples) and the samples
from the handrails of an escalator (10 samples) were
negative. One sample (of 7) from stair handrails was
positive for coronavirus OC43. None of the samples
from toilets (upper surface the toilet bowl lid, button for
flushing, and door lock; 14 samples from different toilets
for each surface type) were positive for any of the tested
respiratory viruses. No respiratory virus was detected in
three samples one from each of the buttons of an eleva-
tor, the trolley handles for luggage or the touch screen
on the check-in machine.
One of the four air samples (25%) from week 5 be-
tween 11:00 h to 11:33 h tested positive for adenovirus.
Among the 10 respiratory virus findings at various sites,
in order of frequency these were rhinovirus (four of ten,
40%, from surfaces); coronavirus (three of ten, 30%, from
surfaces); adenovirus (two of ten, 20%, 1 surface sample, 1
air sample); and influenza A (one of ten, 10%, surface sam-
ple). Subtyping of the influenza A virus by real-time PCR
and by sequencing of the hemagglutinin gene was
attempted but proved unsuccessful.
The Ct-values of the real time PCR readouts ranged
from 36.15 to 41.59.
We performed systematic sampling of frequently
touched surfaces in the passenger pathways of a major
airport during the seasonal influenza epidemic, and de-
tected respiratory virus nucleic acid in 10 % of the sam-
ples. 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 re-
spiratory viruses, and informs planning for preventive
measures to reduce secondary spread. This knowledge
helps in the recognition of hot spots for contact trans-
mission risk, which could be important during an emer-
ging pandemic threat or severe epidemic.
Our main findings identify that respiratory virus con-
tamination of frequently touched surfaces is not uncom-
mon 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 hun-
dred passengers per day. Also, that plastic security trays
are non-porous and virus survival is known to be pro-
In a previous study, environmental sampling for re-
spiratory 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 com-
monly from chair handles . The viral pathogens de-
tected in that study included influenza B virus, human
adenovirus, and human coronavirus OC43/HKU1. In a
different context, a study on virus shedding from pa-
tients 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 . Viral nucleic acid was also detected
in air samples collected around five of 12 (42%) patients.
The presence of viral RNA of pathogens frequently cir-
culating 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 de-
tected for longer than the time for which viability and
transmissibility may persist . 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 rhi-
noviruses, survival times of infective virus and viral RNA
have been reported as > 24 h and > 48 h, respectively .
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
. However, findings from other studies indicate sur-
vival times for SARS and Middle East respiratory syn-
drome coronavirus (MERS-CoV) can be much longer,
Ikonen et al. BMC Infectious Diseases (2018) 18:437 Page 4 of 7
depending on the surface . 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
. Similarly, in Toronto surface samples in a hospital
were positive by PCR for SARS . MERS-CoV has been
shown to remain viable on surfaces for longer than influ-
enza A(H1N1) virus .
We used a PCR panel employed in our standard re-
spiratory 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 limita-
tions because it does not demonstrate the presence of
infective virus, it is commonly used to detect the pres-
ence 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 traf-
fic peaks, well within the reported survival times on sur-
faces 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. , these
are relatively high, suggesting a low viral load on the sur-
faces 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 con-
text. 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 . Killingley and col-
leagues used a logical argument to conclude that their
level of influenza A surface contamination on its own
did not represent an infectious dose . The reasoning
was that as the copy count in their surface samples ap-
proximately only equated to that needed for aerosol
transmission, and the likelihood that higher counts are
required for indirect transmission, their surface contam-
ination doses would not have been infective. In this
study Ct values were similar to Killingley et al. , so
likewise it is reasonable to conclude that the environ-
mental contamination we identified may not always (or
ever) have constituted an infective dose. However, we
are unable to determine precisely when each surface be-
came 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
As previously mentioned, we found the highest fre-
quency of respiratory viruses on plastic trays used in se-
curity 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. Se-
curity trays are highly likely to be handled by all embark-
ing passengers at airports; nevertheless the risk of this
procedure could be reduced by offering hand sanitiza-
tion with alcohol handrub before and after security
screening, and increasing the frequency of tray disinfec-
tion. 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 . 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 unex-
pected, as passengers may pay particular attention to
limiting touch and to hand hygiene, in a washroom en-
vironment. Moreover, we did not conduct tests for any
When an emerging pandemic threat is identified, mea-
sures taken to reduce the risk of transmission in an air-
port, 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  and droplet
transmission), for example in dense queues or at service
counters and immigration procedures, enhancing pro-
motion of hand hygiene and respiratory etiquette, and
possibly arriving traveler screening procedures. The pos-
sible airborne transmission risk can be reduced by en-
suring adequate ventilation to dilute pathogen
concentrations to sufficiently low levels . Guidelines
to mitigate transmission of communicable disease have
been issued by Airports Council International  and
International Civil Aviation Organization , but they
focus on (exit) screening and handling an individual sus-
pected 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 sce-
narios, the majority of cases of emerging infections
would be missed . However, measures preventing
transmission locally could be enhanced, for example by
improving hand sanitization opportunities where in-
tense, repeat touching of surfaces takes place such as im-
mediately before and after security screening, by
enhancing cleaning of frequently touched surfaces, by
Ikonen et al. BMC Infectious Diseases (2018) 18:437 Page 5 of 7
increased use of non-touch devices, or by effective bar-
riers 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 , offering multiple simple possibil-
ities and opportunities for reducing the risk of indirect
Detection of pathogen viral nucleic acids indicates viral
surface contamination at multiple sites associated with
high touch rates, and suggests a potential risk in stand-
ard passenger pathways at airport sites. Security check
trays appear to pose the highest potential risk and are
used by virtually all embarking passengers; they have the
potential to be especially problematic if a severe patho-
gen with an indirect transmission mechanism were to
pose a threat for international spread. Public surface
transport has been shown to be associated with acute re-
spiratory infections , stressing the need to also inves-
tigate the role of various traffic hubs in transmission,
including airports, ports and underground stations.
Ct value: Cycle threshold value; MERS-CoV: Middle East respiratory syndrome
coronavirus; PCR: Polymerase chain reaction; SARS: Severe Acute Respiratory
Syndrome; VTM: Viral transport medium
In addition to the persons listed as authors, the following persons constitute
the PANDHUB consortium: Nadezhda Gotcheva and Raija Koivisto (VTT
Technical Research Centre of Finland Ltd., Tampere, Finland); Anna-Maria Vei-
jalainen (University of Eastern Finland, UEF, Kuopio, Finland); Nicolas Poirot
and Nabila Laajail (Assistance Publique, Paris France); Emma Bennett, Caroline
Walters and Ian Hall (Public Health England, Porton Down, UK); Stephane
Bastier, Yann Lapeyre and Audrey Berthier (MEDES, Toulouse, France).
The collaboration of Heikki Koski at Finavia, managing the Helsinki-Vantaa
Airport, and his colleagues in Finavia is gratefully acknowledged.
The PANDHUB project has received funding from the European Union’s
Seventh Framework Programme for research, technological development
and demonstration under grant agreement no 607433.
Availability of data and materials
All data generated or analysed during this study are included in this
NI, CSK, IK, PP, AS, SS and PR conceived and designed the study and
implemented sampling. NI and CSK supervised laboratory testing and
interpretation. NI, CSK, PR, JE and JVT reviewed the literature. NI, CSK and PR
wrote the first draft of the manuscript, which was commented by all authors.
JE and JVT participated in the analysis and interpretation of data, and revised
the manuscript critically for its intellectual content. All authors read and
approved the final manuscript.
Ethics approval and consent to participate
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Department of Health Security, National Institute for Health and Welfare,
P.O.Box 30, 00271 Helsinki, Finland.
School of Medicine, Division of
Epidemiology and Public Health, University of Nottingham, Nottingham, UK.
VTT Technical Research Centre of Finland Ltd, Espoo and Tampere, Finland.
Department of Environmental and Biological Sciences, University of Eastern
Finland, Kuopio, Finland.
Received: 7 March 2018 Accepted: 15 May 2018
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