Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 26, Number 5—May 2020
Policy Review

Nonpharmaceutical Measures for Pandemic Influenza in Nonhealthcare Settings—International Travel-Related Measures

Sukhyun Ryu, Huizhi Gao, Jessica Y. Wong, Eunice Y.C. Shiu, Jingyi Xiao, Min Whui Fong, and Benjamin J. CowlingComments to Author 
Author affiliations: University of Hong Kong, Hong Kong, China (S. Ryu, H. Gao, J.Y. Wong, E.Y.C. Shiu, J. Xiao, M.W. Fong, B.J. Cowling); Konyang University, Daejeon, South Korea (S. Ryu)

Cite This Article


International travel–related nonpharmaceutical interventions (NPIs), which can include traveler screening, travel restrictions, and border closures, often are included in national influenza pandemic preparedness plans. We performed systematic reviews to identify evidence for their effectiveness. We found 15 studies in total. Some studies reported that NPIs could delay the introduction of influenza virus. However, no available evidence indicated that screening of inbound travelers would have a substantial effect on preventing spread of pandemic influenza, and no studies examining exit screening were found. Some studies reported that travel restrictions could delay the start of local transmission and slow international spread, and 1 study indicated that small Pacific islands were able to prevent importation of pandemic influenza during 1918–19 through complete border closure. This limited evidence base indicates that international travel-related NPIs would have limited effectiveness in controlling pandemic influenza and that these measures require considerable resources to implement.

From time to time, novel influenza A virus strains emerge and cause global influenza pandemics (1). Pandemics occurred 3 times in the 20th century and 1 time so far in the 21st century (2). The recognition that influenza pandemics can have substantial social and economic effects in addition to the impact on public health, along with the emergence of highly pathogenic strains of avian influenza virus in the past 20 years, has stimulated greater attention in preparing for future influenza pandemics (3,4). Given the delays in the availability of specific vaccines and limited supplies of antiviral drugs, nonpharmaceutical interventions (NPIs) form a major part of pandemic plans (2).

A range of NPIs can be applied at international, national, and local levels, with the objectives of delaying the arrival of infected persons, slowing the spread of infection, delaying the epidemic peak, and reducing the size of the peak (5). This article focuses on the use of measures related to international travel, including entry and exit screening of travelers for infection, travel restrictions, and border closures (Table 1). We aimed to review the evidence base assessing the effectiveness of these travel-related NPIs against pandemic influenza and to identify the barriers to implementation of these interventions.

Methods and Results

We searched for literature reporting or estimating the effectiveness of NPIs related to international travel and movement, including entry and exit screening travelers, travel restrictions, and border closures on pandemic or interpandemic influenza. We conducted literature searches on PubMed, Medline, Embase, and Cochrane Library for peer-reviewed articles published from January 1, 1946, through April 28, 2019. The search terms used were identified from relevant systematic reviews and research reports (8,9). We collected additional studies from secondary references from included studies or other relevant searches. Articles were eligible for inclusion if they reported or estimated the effectiveness of international travel–related NPIs for pandemic influenza using quantitative indicators such as delaying the introduction of infection, delaying the epidemic peak, or reducing the size of the peak. We excluded articles if they did not investigate the quantitative effectiveness of international travel–related NPIs or were editorials, reviews, or commentaries without primary data. Furthermore, we restricted articles to those published in English. Two independent reviewers (S.R. and H.G.) screened titles and abstracts and assessed full-text articles for eligibility. A third reviewer (B.J.C.) adjudicated any disagreements between the 2 reviewers.

We extracted the information on the effectiveness of NPIs from included studies by using a structured data-extraction form. Information of interest included the study setting, specific measures implemented, timing of intervention implementation, study results regarding effectiveness indicators, and potential barriers to implementation. The assessment of quality of evidence considered study design and assigned generally higher quality to randomized trials, lower quality to observational studies, and lowest quality to simulation studies. We provide full search terms, search strategies, selection of articles, and summaries of the selected articles (Appendix).

Screening Travelers for Infection

We identified 4 relevant studies that considered the effect of screening on influenza transmission, including 2 epidemiologic studies from the 2009 pandemic (10,11) and 2 simulation studies (12,13). The epidemiologic studies estimated that entry screening delayed the arrival of influenza A(H1N1)pdm09 virus to previously unaffected areas by an average of 7–12 days (11) and delayed the epidemic in China by 4 days by reducing imported cases by 37% from border entry screening (10). The simulation studies predicted that entry screening would delay the arrival of infection into a country by a few days or 1–2 weeks at most (12,13). We did not identify any studies on exit screening; in the 2009 influenza pandemic, exit screening was not implemented by Mexico (14), nor by most other countries.

We did not systematically review studies of the technical performance of various screening tools (e.g., screening case definitions and thermal scanners) but identified in an informal search 4 studies that discussed the challenges of screening travelers for infection, which include limited screening sensitivity (10,11,13), an incubation period of 1–7 days for influenza A(H1N1)pdm09 virus (meaning some infected travelers might not show symptoms until after arrival at their destination) (10,12,13), limited local capacity of influenza surveillance (10,11), and limited public health resources, such as laboratory capacity and funding (10,11,13).

Screening inbound travelers for infection is a very visible public health intervention and can reduce the number of infectious persons entering the country (15). Infrared thermometers are currently used in many ports of entry in Asia because of the instantaneous and noninvasive nature of their use. Several simulation studies (1013) included in this review estimated that this intervention helped to delay the introduction of infected persons. However, the sensitivity of screening travelers has been largely reliant on the sensitivity of detection of fever. Epidemiologic studies (16,17) conducted during the 2009 influenza pandemic demonstrated the low detection rate of entry screening that used the infrared thermal scanner and health declaration form at the airport; the sensitivity of screening travelers for infection was 5.8% in New Zealand and 6.6% in Japan. In addition to the lack of sensitivity for detecting febrile travelers (e.g., some travelers with febrile illness might take antipyretic medicine and evade detection), some infected travelers might travel during the incubation period, which is typically 1–2 days, and thus would not be identified as infected at departure or arrival (10,12). Once infection begins spreading in a local community, identifying additional inbound travelers with infection will do little to limit local spread. In addition, entry screening consumes considerable public health resources, including trained staff, screening devices, and laboratory resources, and thus might not be justifiable (18).

Travel Restrictions

We identified 1 epidemiologic study and 9 simulation studies that estimated or predicted the effectiveness of international travel restrictions (1928) (Table 2). An epidemiologic study estimated that the peak in the number of influenza-associated deaths was delayed by 2 weeks when international flight volume was reduced by 27% (28). Simulation studies predicted that 90%–99% of travel restrictions could delay international spread of cases by 2–19 weeks (20), delay the importation of the first case-patients by 1–8 weeks (2326), and delay the epidemic peak by 1–12 weeks (19,23,24,26,27).

A simulation study predicted that selectively restricting the travel of children could delay the spread of infection by 35 days (R0 = 1.2–2.0) (22), and another simulation study assessing the probability of escaping 1918–19 influenza pandemic among 17 Pacific Island countries and territories estimated that 4–5 countries avoided influenza pandemic (R0 = 1.5–3.0) by strict limitation (79% or 99% restriction) of incoming travelers (21). Three studies explored the barriers to travel restrictions, which included the threat of economic loss (21,26) and lack of compliance among the public (20).

Because the volume of transportation is associated with the spread of influenza (28,30), travel restrictions have been considered as a measure to reduce international spread (31). Although previous expert survey and reviews suggested that travel restrictions are less likely to be effective (8,9,32), international travel restrictions are still included in some national pandemic plans (33). Several of the studies we reviewed (19,20,2228) predicted that international travel restrictions might delay the importation of new infected persons from other affected areas, slow the international spread of the epidemic, and delay the epidemic peak (25). However, simulation studies estimated that travel restrictions after 5 months of the international arrival of the first infected persons would not be effective (26) and that only strict travel restriction was likely to be effective (19); thus, the time of implementation of this measure should be considered with strict travel restrictions at the early stage of a pandemic. Some barriers exist to implementation of travel restrictions against pandemic influenza, most notably the potential economic consequences of restricting business travelers, as well as legal and ethical issues regarding mobility restrictions (34), discrimination of persons from influenza-affected area (35), and lack of public compliance.

Border Closures

One study investigated the effectiveness of border closures in 11 South Pacific Island jurisdictions during the 1918–19 influenza pandemic. We identified 4 islands where strict border control, including 5–7 days of maritime quarantine, substantially delayed the importation of influenza from 3 to 30 months and reduced the mortality rate compared with the other islands that had not implemented border control (36).

Because travel can drive cross-border transmission of infectious diseases, complete border closure could in theory prevent or delay the spread of influenza or its introduction in previously unaffected countries (21,36). However, in practice, complete border closure is likely to be unfeasible, even on isolated islands, because of the need to import food and medical supplies (21), and would result in substantial economic and social disruption (34).


We reviewed the effectiveness of each international travel–related NPI and the barriers to its implementation to provide scientific evidence to public health authorities. Our review found that the effect of screening travelers on entry to a country or region is very limited and unlikely to be a rational use of resources. However, this intervention has a potential role to inform travelers about the risk for infection and provide travel advice on avoiding travel to certain regions after departure or how to seek treatment after arrival (16). Furthermore, such screening can be seen by policy makers and politicians as a visible public health measure to help assure the public that action is being taken (16).

Our review identified the potential threat of economic consequences as a major barrier to implementation of travel restrictions. A simulation study demonstrated that children-selective travel restriction during a pandemic is less likely to affect economic impact compared with nonselective travel restrictions (22). A more structured epidemiologic study is needed to examine the cost and benefit of travel restriction by different risk groups of influenza transmission. A previous study demonstrated that successful border closure for 6 months in an island country provided a net societal benefit of USD 7.3 billion (36). However, this extreme measure is unlikely to be implemented unless required by national law in extraordinary circumstances during a very severe pandemic. The literature on border closure included in our review was based on the historical scenario of the 1918–19 influenza pandemic in isolated islands; this research might have limited relevance given the current and ever increasing levels of globalization.

Although international travel–related NPIs are not likely to be able to prevent importation of pandemic influenza to a country or region, NPIs implemented at the early phase might delay the start of a local epidemic by a few days or weeks (37), which is important if such delay can contribute to reducing the effect of the epidemic (e.g., by buying time to prepare healthcare providers and the public before the arrival of the epidemic, to plan and coordinate social distancing measures, and to purchase additional pharmaceuticals such as antiviral drugs or vaccines) (38). Once an epidemic has started, travel restrictions might also be used to delay the peak of the epidemic in an isolated location where heavy seeding by incoming infected persons could accelerate local transmission. International Health Regulations could play a role in decisions on whether to implement certain international measures (39).

We identified several knowledge gaps that could be filled by further research. Most fundamentally, information is still lacking on some aspects of the basic epidemiology of influenza, including the dynamics of person-to-person transmission (e.g., Can a person be infectious before the onset of symptoms? Can transmission occur from an asymptomatic or pauci-symptomatic case-patient? What fraction of infections are asymptomatic?). In terms of specific research on the effectiveness of travel-related NPIs, it is difficult to envisage how intervention studies could be done, but epidemiologic studies could be planned in advance of influenza pandemics or perhaps severe influenza epidemics. Studies could answer questions such as how many infections are imported from overseas or whether travel advisories might encourage infected persons not to travel.

Our review needs to be interpreted in light of some limitations. First, although international travel or trade of infected animals might have a role in the international spread of influenza, the study that assessed the movement restriction of animals was not included in this review. Second, mathematical models are useful tools for investigating the advantages and disadvantages of different interventions, but the results often depend on key modeling assumptions that are difficult to verify (19). The assessment of the quality of evidence was considered weak overall, given that most of the epidemiologic studies included in our review were ecologic studies. Third, only a few studies on the ethical and economic considerations regarding travel-related measures during influenza epidemics and pandemics were available (26,40).

Many countries continue to update their influenza pandemic plans on the basis of the latest available evidence. We found that international travel–related NPIs could delay the introduction of influenza and delay the start of local transmission; however, limited evidence exists to inform the use of these NPIs for controlling pandemic influenza. The evidence that we identified in our review does not support entry screening as an efficient or effective measure, and travel restrictions and border closures are likely to be too disruptive to consider. Additional prospective research on the effectiveness of travel-related NPIs would be valuable to support evidence-based decisions for future influenza pandemics.

Dr. Ryu is an assistant professor of preventive medicine at Konyang University, Daejeon, South Korea. His research interests include infectious disease epidemiology, with a focus on influenza and public health interventions.



This work was conducted in preparation for the development of guidelines by the World Health Organization on the use of nonpharmaceutical interventions for pandemic influenza in nonmedical settings and was financially supported by the World Health Organization.



  1. Dawood  FS, Jain  S, Finelli  L, Shaw  MW, Lindstrom  S, Garten  RJ, et al.; Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med. 2009;360:260515. DOIPubMedGoogle Scholar
  2. The Lancet Infectious Diseases. The Lancet Infectious Diseases. How to be ready for the next influenza pandemic. Lancet Infect Dis. 2018;18:697. DOIGoogle Scholar
  3. Smith  RD, Keogh-Brown  MR, Barnett  T, Tait  J. The economy-wide impact of pandemic influenza on the UK: a computable general equilibrium modelling experiment. BMJ. 2009;339(nov19 1):b4571.
  4. World Health Organization. Draft thirteenth general programme of work, 2019–2023. 2018 [cited 2019 Jul 10].
  5. Bell  D, Nicoll  A, Fukuda  K, Horby  P, Monto  A, Hayden  F, et al.; World Health Organization Writing Group. Non-pharmaceutical interventions for pandemic influenza, national and community measures. Emerg Infect Dis. 2006;12:8894.PubMedGoogle Scholar
  6. European Centre for Disease Prevention and Control. Infection prevention and control measures for Ebola virus disease: entry and exit screening measures. 2014 [cited 2019 Jul 10].
  7. US Homeland Security Council. National strategy for pandemic influenza implementation plan. 2006 [cited 2019 Jul 10].
  8. Mateus  AL, Otete  HE, Beck  CR, Dolan  GP, Nguyen-Van-Tam  JS. Effectiveness of travel restrictions in the rapid containment of human influenza: a systematic review. Bull World Health Organ. 2014;92:868880D. DOIPubMedGoogle Scholar
  9. Lee  VJ, Lye  DC, Wilder-Smith  A. Combination strategies for pandemic influenza response - a systematic review of mathematical modeling studies. BMC Med. 2009;7:76. DOIPubMedGoogle Scholar
  10. Yu  H, Cauchemez  S, Donnelly  CA, Zhou  L, Feng  L, Xiang  N, et al. Transmission dynamics, border entry screening, and school holidays during the 2009 influenza A (H1N1) pandemic, China. Emerg Infect Dis. 2012;18:75866. DOIPubMedGoogle Scholar
  11. Wu  JT, Cowling  BJ, Lau  EH, Ip  DK, Ho  LM, Tsang  T, et al. School closure and mitigation of pandemic (H1N1) 2009, Hong Kong. Emerg Infect Dis. 2010;16:53841. DOIPubMedGoogle Scholar
  12. Caley  P, Becker  NG, Philp  DJ. The waiting time for inter-country spread of pandemic influenza. PLoS One. 2007;2:e143. DOIPubMedGoogle Scholar
  13. Malone  JD, Brigantic  R, Muller  GA, Gadgil  A, Delp  W, McMahon  BH, et al. U.S. airport entry screening in response to pandemic influenza: modeling and analysis. Travel Med Infect Dis. 2009;7:18191. DOIPubMedGoogle Scholar
  14. Khan  K, Eckhardt  R, Brownstein  JS, Naqvi  R, Hu  W, Kossowsky  D, et al. Entry and exit screening of airline travellers during the A(H1N1) 2009 pandemic: a retrospective evaluation. Bull World Health Organ. 2013;91:36876. DOIPubMedGoogle Scholar
  15. Read  JM, Diggle  PJ, Chirombo  J, Solomon  T, Baylis  M. Effectiveness of screening for Ebola at airports. Lancet. 2015;385:234. DOIPubMedGoogle Scholar
  16. Hale  MJ, Hoskins  RS, Baker  MG. Screening for influenza A(H1N1)pdm09, Auckland International Airport, New Zealand. Emerg Infect Dis. 2012;18:8668. DOIPubMedGoogle Scholar
  17. Sakaguchi  H, Tsunoda  M, Wada  K, Ohta  H, Kawashima  M, Yoshino  Y, et al. Assessment of border control measures and community containment measures used in Japan during the early stages of Pandemic (H1N1) 2009. PLoS One. 2012;7:e31289. DOIPubMedGoogle Scholar
  18. Priest  PC, Jennings  LC, Duncan  AR, Brunton  CR, Baker  MG. Effectiveness of border screening for detecting influenza in arriving airline travelers. Am J Public Health. 2013;103:14128. DOIPubMedGoogle Scholar
  19. Ferguson  NM, Cummings  DA, Fraser  C, Cajka  JC, Cooley  PC, Burke  DS. Strategies for mitigating an influenza pandemic. Nature. 2006;442:44852. DOIPubMedGoogle Scholar
  20. Hollingsworth  TD, Ferguson  NM, Anderson  RM. Will travel restrictions control the international spread of pandemic influenza? Nat Med. 2006;12:4979. DOIPubMedGoogle Scholar
  21. Eichner  M, Schwehm  M, Wilson  N, Baker  MG. Small islands and pandemic influenza: potential benefits and limitations of travel volume reduction as a border control measure. BMC Infect Dis. 2009;9:160. DOIPubMedGoogle Scholar
  22. Lam  EH, Cowling  BJ, Cook  AR, Wong  JY, Lau  MS, Nishiura  H. The feasibility of age-specific travel restrictions during influenza pandemics. Theor Biol Med Model. 2011;8:44. DOIPubMedGoogle Scholar
  23. Bajardi  P, Poletto  C, Ramasco  JJ, Tizzoni  M, Colizza  V, Vespignani  A. Human mobility networks, travel restrictions, and the global spread of 2009 H1N1 pandemic. PLoS One. 2011;6:e16591. DOIPubMedGoogle Scholar
  24. Ciofi degli Atti  ML, Merler  S, Rizzo  C, Ajelli  M, Massari  M, Manfredi  P, et al. Mitigation measures for pandemic influenza in Italy: an individual based model considering different scenarios. PLoS One. 2008;3:e1790. DOIPubMedGoogle Scholar
  25. Epstein  JM, Goedecke  DM, Yu  F, Morris  RJ, Wagener  DK, Bobashev  GV. Controlling pandemic flu: the value of international air travel restrictions. PLoS One. 2007;2:e401. DOIPubMedGoogle Scholar
  26. Chong  KC, Ying Zee  BC. Modeling the impact of air, sea, and land travel restrictions supplemented by other interventions on the emergence of a new influenza pandemic virus. BMC Infect Dis. 2012;12:309. DOIPubMedGoogle Scholar
  27. Cooper  BS, Pitman  RJ, Edmunds  WJ, Gay  NJ. Delaying the international spread of pandemic influenza. PLoS Med. 2006;3:e212. DOIPubMedGoogle Scholar
  28. Brownstein  JS, Wolfe  CJ, Mandl  KD. Empirical evidence for the effect of airline travel on inter-regional influenza spread in the United States. PLoS Med. 2006;3:e401. DOIPubMedGoogle Scholar
  29. McLeod  MA, Baker  M, Wilson  N, Kelly  H, Kiedrzynski  T, Kool  JL. Protective effect of maritime quarantine in South Pacific jurisdictions, 1918-19 influenza pandemic. Emerg Infect Dis. 2008;14:46870. DOIPubMedGoogle Scholar
  30. Fang  LQ, Wang  LP, de Vlas  SJ, Liang  S, Tong  SL, Li  YL, et al. Distribution and risk factors of 2009 pandemic influenza A (H1N1) in mainland China. Am J Epidemiol. 2012;175:8907. DOIPubMedGoogle Scholar
  31. Wood  JG, Zamani  N, MacIntyre  CR, Beckert  NG. Effects of internal border control on spread of pandemic influenza. Emerg Infect Dis. 2007;13:103845. DOIPubMedGoogle Scholar
  32. Aledort  JE, Lurie  N, Wasserman  J, Bozzette  SA. Non-pharmaceutical public health interventions for pandemic influenza: an evaluation of the evidence base. BMC Public Health. 2007;7:208. DOIPubMedGoogle Scholar
  33. World Health Organization. Comparative analysis of national pandemic influenza preparedness plans. 2011 [cited 2019 Jul 10].
  34. World Health Organization. Ethical consideration in developing a public health response to pandemic influenza. 2007 [cited 2019 Jul 10].
  35. World Health Organization. Guidance for managing ethical issues in infectious disease outbreaks. 2016 [cited 2019 Jul 10].
  36. Boyd  M, Baker  MG, Mansoor  OD, Kvizhinadze  G, Wilson  N. Protecting an island nation from extreme pandemic threats: Proof-of-concept around border closure as an intervention. PLoS One. 2017;12:e0178732. DOIPubMedGoogle Scholar
  37. Bell  D, Nicoll  A, Fukuda  K, Horby  P, Monto  A, Hayden  F, et al.; World Health Organization Writing Group. Non-pharmaceutical interventions for pandemic influenza, international measures. Emerg Infect Dis. 2006;12:817. DOIPubMedGoogle Scholar
  38. World Health Organization. Pandemic influenza risk management. 2017 [cited 2019 Jul 10].
  39. World Health Organization. International Health Regulations (2005), 3rd edition. 2016 [cited 2019 Jul 10].
  40. Saunders-Hastings  P, Crispo  JAG, Sikora  L, Krewski  D. Effectiveness of personal protective measures in reducing pandemic influenza transmission: A systematic review and meta-analysis. Epidemics. 2017;20:120. DOIPubMedGoogle Scholar




Cite This Article

DOI: 10.3201/eid2605.190993

Original Publication Date: February 06, 2020

Table of Contents – Volume 26, Number 5—May 2020

EID Search Options
presentation_01 Advanced Article Search – Search articles by author and/or keyword.
presentation_01 Articles by Country Search – Search articles by the topic country.
presentation_01 Article Type Search – Search articles by article type and issue.



Please use the form below to submit correspondence to the authors or contact them at the following address:

Benjamin J. Cowling, WHO Collaborating Centre for Infectious Disease Epidemiology and Control, School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, 1/F Patrick Manson Building (North Wing), 7 Sassoon Rd, Hong Kong, China

Send To

10000 character(s) remaining.


Page created: April 16, 2020
Page updated: April 16, 2020
Page reviewed: April 16, 2020
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.