INTRODUCTION

The transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) via air travel has complicated global public health policy. The World Health Organization has determined that the rapid spread of the disease in 2020 may have been partially due to the initial absence of flight screening and quarantine procedures for travelers [1]. The emergence of infectious SARS-CoV-2 strain has necessitated the implementation of both non-pharmaceutical and pharmaceutical interventions to curb transmission. Given the endemic nature of SARS-CoV-2, evaluating these approaches is essential to confirm their effectiveness in preventing transmission through key vectors, including air passengers [2]. This need is further emphasized by the impracticality and impossibility of achieving herd immunity due to the continuous evolution of vaccine-resistant strains, non-adherence to vaccination schedules, and the resumption of pre-pandemic travel behaviors. An in-depth understanding of the efficacy of travel screening, testing, and quarantine mandates is crucial to inform future strategies for managing SARS-CoV-2 and potential future respiratory viral infections.

The overall risk of in-flight transmission of SARS-CoV-2 among passengers is considered minimal because aircraft are equipped with high-efficiency particulate-absorbing filtration and air circulation systems [3]. This observation aligns with the patterns noted during the original severe acute respiratory syndrome outbreak [4]. However, genomic testing indicates that transmission between air passengers is possible [5] and influenced by several behavioral factors, such as proximity to infected individuals, patterns of passenger movement, and masking behaviors [3,6,7]. It is crucial to assess the potential impact of clusters of SARS-CoV-2 infections among air passengers in the countries that receive these travelers [8].

Pre-departure reverse-transcriptase polymerase chain reaction (RT-PCR) testing has demonstrated variable effectiveness in detecting SARS-CoV-2 among passengers. This inconsistency is often linked to the time between testing and the flight, which may allow for recent exposure and infection [9,10]. Nonetheless, RT-PCR is considered to have high specificity for identifying positive cases of SARS-CoV-2 [11]. Pre-travel screening methods, such as body temperature measurements and symptom-based questionnaires, generally prove ineffective on their own. This is largely due to the high number of asymptomatic infections and the variable presentation of fevers among those infected [9]. Asymptomatic carriers, who can still transmit the virus, represent a significant risk for person-to-person transmission on board an aircraft [12]. Mandatory mask-wearing policies during flights have been effective in lowering the rates of infection transmission [6]. However, the lack of uniformity in implementing safe flying guidelines by airlines has resulted in diverse policies concerning masking, testing, and the disinfection process of airplanes [13].

Post-arrival screening alone has been found to be ineffective, mirroring the limitations observed with pre-departure screening methods [14]. However, enforcing mandatory quarantine for travelers in designated facilities, rather than at home, effectively prevents the spread of disease to the local community [14]. During the implementation of international travel restrictions, mandatory hotel quarantines not only mitigated the risk of importing infections but also supported the economic stability of tourism-dependent sectors worldwide [9]. In nations that implemented a combination of pre-departure testing, post-arrival testing, mandatory quarantine with periodic testing, and isolation of infected individuals, researchers recognized the potential to effectively prevent SARS-CoV-2 transmission among passengers and establish travel corridors free from SARS-CoV-2 [9]. The effectiveness of screening in conjunction with mandatory quarantine in identifying both symptomatic and asymptomatic cases and in reducing transmission rates has been demonstrated [14]. However, it is important to note that most studies assessing the risk of contracting SARS-CoV-2 through these methods are based on modeling, field epidemiological investigations, or small observational studies. These studies have inherent design limitations that may hinder researchers’ ability to extrapolate their findings to the broader population at risk [5,6,8,10,12,15].

This study aimed to validate the risk of SARS-CoV-2 and identify infection risk factors among at-risk air passengers with a 14-day mandatory quarantine. Additionally, the effectiveness of mass symptom-based screening criteria at airports was evaluated.

METHODS

Study Design and Setting

This retrospective cohort study analyzed air passengers arriving in Thailand through Suvarnabhumi Airport (International Air Transport Association code: BKK) from April 2020 to September 2020. The objective was to assess the transmissibility of SARS-CoV-2 and evaluate the effectiveness of post-arrival screening and mandatory quarantine policies. Suvarnabhumi Airport, which handles the highest volume of air traffic in Thailand, served as the primary entry point for air travelers following the implementation of the SARS-CoV-2 travel restriction policy by the Thai government in April 2020.

Eligibility criteria for travel were established by the Center for COVID-19 Situation Administration (CCSA) under Section 9 of the Emergency Decree on Public Administration in Emergency Situations B.E. 2548 (2005). Both Thai and non-Thai air passengers were eligible to fly to Thailand for approved purposes, provided they met pre-arrival preparation requirements. These included undergoing a pre-departure RT-PCR test within 72 hours, obtaining a Fit to Fly Certificate from a medical professional, and receiving a Certificate of Entry (COE) from the Department of Consular Affairs, Ministry of Foreign Affairs of Thailand. Non-Thai nationals had to submit a detailed travel plan, provide proof of health insurance with coverage of at least US$100 000, and obtain a Letter of Approval for quarantine accommodation from Thai CCSA-designated facilities. Additionally, non-Thai passengers were required to provide booking information for an approved quarantine hotel before a COE could be issued. All non-Thai nationals were required to present a SARS-CoV-2 RT-PCR test result showing undetectable levels of the virus, taken within 72 hours prior to departure. While this was also encouraged for Thai nationals, it was not mandatory. However, all passengers had to undergo pre-boarding symptom screening. In-flight protocols mandated that both passengers and crews wear masks throughout the flight. Social distancing measures were also enforced, with passengers seated with one empty space between each other in the same row and staggered seating across different rows. This arrangement ensured that no passenger had another seated directly in front of or behind them.

The Division of International Communicable Disease Control Ports and Quarantine in Thailand was tasked with implementing symptom-based screening for all international arrivals at Suvarnabhumi Airport. Upon arrival, air passengers underwent screening at airport checkpoints through direct interviews and temperature checks using handheld infrared thermometers. Those who tested positive in this initial screening and met the defined criteria were designated as patients under investigation (PUI). Passengers with a forehead temperature exceeding 36.8°C (98.24°F), as measured by a handheld thermometer, underwent a secondary check using an in-ear thermometer. If this second measurement showed a temperature of 37.3°C (99.14°F) or higher, the passenger was classified as a PUI. The rationale for setting the forehead temperature cutoff at 36.8ºC was to minimize the risk of false negatives, thereby capturing more potential cases before confirmation with the in-ear temperature. Additionally, any passenger who reported symptoms of SARS-CoV-2 (such as cough, sore throat, runny nose, distorted sense of smell, or shortness of breath) within the 14 days prior to arrival, including at the time of the interview, was also identified as a PUI. All identified PUIs had specimens collected via swab at the airport, which were then sent to external reference laboratories for testing. While awaiting these results, PUIs were directed to local hospitals for isolation. PUIs who tested positive for SARS-CoV-2 were treated at local hospitals. Those with negative results were referred to state, alternative, or hospital alternative state quarantine facilities. Individuals not identified as PUIs were directed to state, alternative, or hospital quarantine as well (Figure 1).

Quarantine facilities were established in participating hotels to accommodate air passengers during the initial 14-day quarantine period. All individuals were required to undergo state, alternative, or hospital quarantine based on their eligibility criteria. Most Thai nationals were placed in state quarantine, while non-Thai and self-paying Thai air passengers were offered alternative quarantine. Hospital quarantine was available to individuals traveling to Thailand for medical care, provided they were free of coronavirus disease 2019 (COVID-19). All passengers underwent SARS-CoV-2 testing via RT-PCR at least twice during the quarantine. The first PCR test was administered within 3–5 days of arrival, and the second test between 11–13 days after arrival in Thailand. Participants were also required to download and use a tracing application to monitor symptoms and ensure compliance with quarantine regulations; those reporting symptoms underwent additional testing for SARS-CoV-2. Following the 14-day quarantine, participants who tested negative for SARS-CoV-2 via RT-PCR were released into the community and allowed to travel freely within the country.

Study Participants

All air passengers who entered Thailand via Suvarnabhumi Airport from April 2020 to September 2020 were included in the study. To enter Thailand by air, passengers were required to provide the documents and information specified by the Center for COVID-19 Situation Administration.

Data Collection

This study utilized data from multiple sources to triangulate and validate the values obtained for each air passenger. Passengers’ data, including sex, age, and country of departure, was provided by the Immigration Bureau at Suvarnabhumi Airport. Data regarding the criteria for disease investigation, SARS-CoV-2 test results, sex, age, symptoms reported by passengers during quarantine, and country of origin for individuals identified as PUIs were provided by the Ministry of Public Health Thailand. The number of people quarantined in government-designated facilities and the number of infected individuals detected during quarantine was provided by the Ministry of Defense Thailand. Disease investigation information about patients with positive SARS-CoV-2 status while in quarantine, including sex, age, country of origin, clinical information, and risk history, was provided by the Bureau of Epidemiology. All country-of-departure data was sorted into regional data using the World Health Organization region map.

Statistical Analysis

Descriptive statistics were used to present the characteristics of the passengers. Incidence rates were computed and categorized by sex, nationality, continent of departure, PUI status, and travel month. The statistical differences in incidence among subgroups were assessed using an exact probability test and chi-squared test, as appropriate. Factors associated with the risk of SARS-CoV-2 detection were examined through Poisson regression with robust standard errors. Screening accuracy indices, including sensitivity and specificity, were determined to assess the efficacy of the symptom-based screening system.

Ethics Statement

This study received approval from the Ethics Committee for Research Related to COVID-19 Disease or Public Health Emergency, Department of Disease Control, Ministry of Public Health, Thailand (FWA 00013622).

RESULTS

Of the 116 004 air passengers screened, 626 tested positive for SARS-CoV-2 during the screening and quarantine process. The screening identified 1369 individuals as PUIs; of these, 77 tested positive for SARS-CoV-2 at the airport, while the remaining 549 positive cases were detected during quarantine (Figure 2).

The overall cumulative incidence was 540 infected individuals per 100 000 air passengers (0.5%). The age range of the study population spanned from less than 1 year to 99 years old. The average age of air passengers who tested positive for SARS-CoV-2 was 32.7 years, which was significantly lower by 3.5 years compared to those who tested negative. The incidence among males was 0.7%, significantly higher than that among females. Thai nationals comprised 62.6% of the study population, and the incidence among Thais was significantly higher than that among non-Thais. Thai nationals accounted for 85.0% of the 626 infected cases. The majority of passengers (51.5%) departed from the Western Pacific Region (WPR), while the smallest percentage of passengers departed from the African Region (AFR) at 0.6%. The WPR had the lowest incidence of SARS-CoV-2 detection at 0.1%; the Region of the Americas (AMR) experienced the highest incidence at 7.5% (Supplemental Material 1). An analysis of symptom-based screening revealed that 1.2% of all air passengers screened positive and were designated as PUIs upon arrival; 5.6% of these PUIs tested positive for SARS-CoV-2 via RT-PCR. Eight PUIs who initially tested negative for SARS-CoV-2 upon arrival were later confirmed positive during the quarantine period. Among the infected, 87.7% were non-PUIs; 12.3% of the infected individuals were assigned PUI status based on symptom-based screening upon arrival. When stratified by month, the volume of passengers increased month-by-month over the study period, while the incidence remained relatively constant, except for a noticeable decrease in August (Table 1).

The countries with the highest and lowest numbers of departing passengers were the United Arab Emirates (n=15 786) and Madagascar (n=1), respectively. The top five countries of departure with the highest number of infected cases included Bhutan (n=92), Trinidad and Tobago (n=54), Djibouti (n=50), Saudi Arabia (n=41), and Libya (n=40). All passengers returning from South Sudan tested positive for SARS-CoV-2 (Supplemental Material 2).

Males were 2.18 times the risk of contracting SARS-CoV-2 than females. Individuals of non-Thai nationality had a 0.28 times the risk of contracting SARS-CoV-2 than those of Thai nationality. Using the South-East Asia Region as the reference, passengers departing from the WPR and European Region (EUR) exhibited a significantly lower risk of SARS-CoV-2 infection, whereas passengers from all other regions faced a higher risk. Individuals designated as PUIs were 7.70 times the risk of being detected for SARS-CoV-2 infection than non-PUIs. Using April as the reference month, the risk was not statistically significantly different except in September; air passengers traveling in September were at a 3.70 times the risk of contracting SARS-CoV-2 (Table 2).

An examination of the on-arrival symptoms screening process revealed that the screening criteria had a sensitivity of 13.6% and a specificity of 98.9%. All PUIs exhibited symptoms commonly associated with SARS-CoV-2. The area under the receiver operating characteristic (ROC) curve was 0.56. The positive likelihood ratio stood at 12.2. The positive predictive value was 6.2% and the negative predictive value was 99.5% (Table 3).

DISCUSSION

The overall infection rate of SARS-CoV-2 among the 116 004 air passengers was 0.5%, or approximately five cases per 1000 passengers. This rate reflects the risk of SARS-CoV-2 infection after initial pre-departure screening of passengers during the early stages of the COVID-19 pandemic, before pharmaceutical preventative measures were widely available, thus representing the inherent risk without the influence of vaccines. Key risk factors for SARS-CoV-2 infection among air passengers included male sex, Thai nationality, departure from non-WPR and non-EUR regions, PUI status, and travel during September 2020. The sensitivity of symptom-based screening criteria was found to be low. Although PUI status was associated with a higher risk of detecting SARS-CoV-2, the sensitivity and area under the ROC curve indicated that symptom-based screening criteria were not consistently effective in identifying positive cases of SARS-CoV-2.

Previous modeling and smaller epidemiological field investigations have estimated that the risk of SARS-CoV-2 transmission during air travel is low [3,7,16]. This study’s findings, which identified the real-world incidence of SARS-CoV-2 among air passengers, support these earlier estimates [13,16]. By utilizing quarantine data to determine incidence rates, this study helped validate the conclusions regarding the overall infection risk presented in previous research, benefiting from the large sample size analyzed. However, it is important to note that this risk assessment is based on the implementation of multiple mandatory non-pharmaceutical preventative measures. The actual risk of air travel could be higher without these measures in place. As many of these preventative policies have been discontinued, there remains a potential risk for the cross-border importation of SARS-CoV-2 cases, which could lead to local outbreaks.

In this study, male passengers exhibited a higher risk of SARS-CoV-2 infection compared to female passengers. Male sex may act as a risk factor for SARS-CoV-2 infection in adults, potentially due to both biological and lifestyle factors [17].

Generally, older individuals are at a higher risk of SARS-CoV-2 infection; however, air passengers aged 60 years and older experienced the lowest incidence of SARS-CoV-2 and were not at a higher risk of contracting the virus than other age groups in this study [17]. It is plausible that individuals in this age group adhere more consistently to recommended precautions, such as wearing masks and maintaining social distancing, compared to younger groups due to their increased risk of infection and severe disease from SARS-CoV-2 [18,19].

The number of Thai participants exceeded that of non-Thai participants, a disparity likely influenced by entry restrictions into Thailand and the necessity for repatriation flights during this period. Non-Thai nationals exhibited a lower risk of contracting SARS-CoV-2 compared to Thai natives. This difference in risk levels could be due to varying pre-departure testing protocols; specifically, Thai nationals were not mandated to provide a negative RT-PCR test before departure.

Passengers departing from the AFR and AMR regions experienced the highest risk of SARS-CoV-2 infection, which may be linked to the higher incidence rates observed in countries within these continents. It is crucial to note that these individuals were passengers who departed from these countries, not necessarily citizens of these countries. This observation could explain the high number of passengers departing from the United Arab Emirates, given that Dubai serves as a major flight transfer hub in the EMR region. However, the availability of incidence data for these continents and countries is limited, which restricts our ability to compare the incidence rates observed in the study with those of the corresponding continents and countries. The increased risk could be attributed to inadequate SARS-CoV-2 control measures in these nations or continents. Furthermore, longer flight durations from more distant destinations may also contribute to the heightened risk of SARS-CoV-2 infection.

The incidence of SARS-CoV-2 remained stable month to month, despite a noticeable increase in travel volume throughout the study period. This stability indicates that the incidence rate is consistent among varying sizes of air passenger populations. However, it was observed that individuals who traveled in September 2020 faced a significantly higher risk of contracting SARS-CoV-2 compared to other months. This heightened risk could be linked to the surge in travel volume. Additionally, the increase in the number of weekly cases globally during September 2020, relative to earlier months, may have also contributed to this elevated risk [20].

The analysis of symptomatic screening criteria used to identify potentially infected individuals upon arrival suggested that, although individuals identified as PUIs experienced a higher risk of SARS-CoV-2 infection, the screening criteria could not consistently identify individuals with SARS-CoV-2. This inconsistency is likely due to the variable incubation period and prevalence of asymptomatic infection, as these individuals would likely not present with symptoms at the screening [21]. This finding corroborates previous findings, as symptom-based screening procedures generally display a low area under the ROC curve and may not consistently identify positive cases [22]. Traditionally, screening processes have relied upon symptomatic evidence of infection to identify potentially infected individuals [23]. However, given the inconsistency of the effectiveness of symptom-based screening criteria for identifying SARS-CoV-2 cases, incorporating additional non-symptom-based patient characteristics related to SARS-CoV-2 infection may assist in increasing sensitivity and area under the ROC curve while maintaining the strengths of the symptomatic screening criteria. Further investigation is needed to determine what added criteria may create this effect. With this in mind, symptom-based screening systems show usefulness in identifying symptomatic cases for isolation and treatment. However, given that our symptom-based screening process was combined with a 14-day mandatory hotel quarantine system, it appeared that almost all positive cases could be isolated and treated before entering the community. This finding is also consistent with prior knowledge, as combined pre-departure testing, testing on arrival, and mandatory quarantine with testing approaches towards infection control have been estimated to be the most effective and had the potential to create SARS-CoV-2 free travel spaces [9].

The primary strength of this study lies in its analysis of a large population. However, a limitation was the inability to fully confirm that Thai nationals were free of SARS-CoV-2 at the beginning of the study, as there was no requirement for pre-departure testing. This issue was partially addressed through the Fit-to-Fly Certificate, pre-departure screening requirements, and the promotion of optional RT-PCR testing. Nonetheless, the study successfully determined the real-world incidence of SARS-CoV-2 among air passengers after initial pre-departure screening, identified risk factors for infection, and evaluated the effectiveness of symptom-based screening criteria. These findings may guide future strategies for pandemic control and provide insights into the risks associated with air travel during viral respiratory disease outbreaks. It is recommended that cross-border infection control policies incorporate traditional quarantine models alongside both symptomatic and asymptomatic disease screening. This approach will help identify and manage viral respiratory diseases, regardless of symptom presentation, and prevent the importation of infections that could lead to local outbreaks.

Supplemental Materials

Notes

Conflict of Interest

The authors have no conflicts of interest associated with the material presented in this paper.

Funding

None.

Author Contributions

Conceptualization: Direkwutthikun T, Rojanaworarit C, Hunsajarupan B, Buathong R. Data curation: Direkwutthikun T, Jannok T, Sookchom P, Photisan N. Formal analysis: Rojanaworarit C, Photisan N, Sookchom P. Funding acquisition: None. Methodology: Direkwutthikun T, Rojanaworarit C, Hunsajarupan B, Andrade I, Photisan N. Project administration: Direkwutthikun T, Rojanaworarit C. Writing – original draft: Andrade I, Rojanaworarit C. Writing – review & editing: Direkwutthikun T, Rojanaworarit C, Hunsajarupan B, Andrade I, Photisan N, Buathong R.

Acknowledgements

Figure 1

Symptom-based screening system for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection on arrival at airport. COVID-19, coronavirus disease 2019; RT-PCR, reverse-transcriptase polymerase chain reaction.

Figure 2

Flow of air passengers through on-arrival airport screening and 14-day quarantine procedures. PUI, patient under investigation; RT-PCR, reverse-transcriptase polymerase chain reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2; COVID-19, coronavirus disease 2019.

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Figure & Data

References

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