Screening for influenza A(H1N1)pdm09, Auckland International Airport, New Zealand.

Entry screening for influenza A(H1N1)pdm09 at Auckland International Airport, New Zealand, detected 4 cases, which were later confirmed, among 456,518 passengers arriving April 27–June 22, 2009. On the basis of national influenza surveillance data, which suggest that ≈69 infected travelers passed through the airport, sensitivity for screening was only 5.8%.

T he virus that caused the 2009 infl uenza pandemic, hereafter referred to as infl uenza A(H1N1)pdm09, is mainly spread internationally by air travel (1). To prevent or delay such spread, during the pandemic many countries initiated screening of air travelers arriving at airports, even though these measures have not been recommended by the World Health Organization (2). On April 25, 2009, New Zealand was one of the fi rst countries outside the Americas to confi rm infl uenza A(H1N1)pdm09 in arriving airline passengers (3). During April 27-June 22, 2009, at the direction of the Ministry of Health, the Auckland Regional Public Health Service began a screening program at Auckland International Airport.
Protocols for border screening were updated throughout the pandemic and evolved as new information became available. Screening was initially applied to all passengers arriving or transferring on fl ights from countries where community transmission of infl uenza A(H1N1)pdm09 virus was occurring. The screening program included the following ( Figure): • All fl ights notifi ed New Zealand of the health of passengers and crew on board before landing; if indicated, the aircraft was met by public health offi cials who triaged these travelers.
• Cabin crew announced a scripted health message requesting passengers to identify themselves if symptomatic; after disembarkation, all passengers passed through a public health checkpoint where signage encouraged ill travelers to seek screening.
• Information about infl uenza A(H1N1)pdm09 was available, those with symptoms could self-declare, and public health offi cials visually inspected arriving passengers and approached those with apparent symptoms.
• Neither thermal scanning nor active screening of every arriving passenger was used.
Each unwell passenger and crew member was screened for infl uenza-like illness by a nurse and assessed by a medical offi cer if illness met the defi nition of a suspected case. Those whose illness met the case defi nition had nasopharyngeal swabs taken, were offered oseltamivir, and were sent home or to a facility for isolation. Reverse transcription PCR (RT-PCR) was used to confi rm infection. Screening was escalated on April 29 to include all passengers arriving from other countries and stopped on June 22.

The Study
We quantifi ed the results of entry screening for infl uenza A(H1N1)pdm09 at Auckland International Airport. Using the information generated during screening, we retrospectively estimated the number of infected travelers who actually passed through the airport. To estimate the sensitivity of screening, we then compared screening fi ndings with the expected number of infected travelers who passed through the airport. Ethical approval was received from the Northern X Regional Ethics Committee of the New Zealand Ministry of Health.
The number of screened passengers was obtained from airport records. The numbers of crew members on inbound international aircraft were estimated by using averages for fl ights into Auckland. The number of travelers detected at each step and referred to the next step of the screening process was obtained from Auckland Regional Public Health Service records. Virologic test results were extracted from laboratory information systems. A confi rmed case was one that met the current case defi nition (as published on the Ministry of Health website, www.health.govt.nz) and one for which RT-PCR result was positive.
We estimated the number of infected travelers screened as the total number of confi rmed cases in New Zealand during this period, multiplied by the proportion of overseas-acquired cases, and the proportion of international travelers arriving at the airport. On April 30, 2009, nonseasonal infl uenza A (H1N1) was made notifi able,  (4). During the screening period, 456,518 international travelers were screened; 406 (0.09%) of these were referred for medical assessment. Of those, 109 (27%) met the case defi nition and received virologic testing. RT-PCR results were located for 89 (82%), among which 4 were positive. A total of 312 cases were confi rmed. The proportion of travelers who acquired the infection overseas was 32%. The proportion who passed through the airport was 69%. The expected number of infected travelers estimated to have passed through the border during the screening program was therefore 69, giving an estimated sensitivity of 5.8% (95% CI 2.3%-14.0%).

Conclusions
The infl uenza A(H1N1)pdm09 screening program at Auckland International Airport had low sensitivity. This form of border screening is therefore unlikely to have substantially delayed spread of the pandemic into New Zealand in 2009.
Limitations of infl uenza screening include the high proportion of asymptomatic infected travelers (5), incubation of infections acquired before or during a fl ight (3), reliance on self-identifi cation, limitations of case defi nitions, and limitations of thermal scanning (6). Modeling data have shown that the ability of border screening to delay global pandemic infl uenza is closely linked to the effectiveness of the screening process or travel restriction used. To delay infl uenza spread by 1.5 weeks, border restrictions need to reduce imported infections by 90% (7). The entry screening program we describe does not meet these standards.
The potential effectiveness of screening arriving travelers to prevent or delay infl uenza epidemics has been debated. Mathematical models and literature reviews have argued for (7,8) and against (9-11) this approach. Some authors have found that entry screening for respiratory conditions or infl uenza A(H1N1)pdm09 is insensitive and not cost-effective (12). Border screening did not substantially delay local transmission of infl uenza A(H1N1) pdm09 (13).
This study has several limitations, particularly with regard to estimating the number of infected travelers who would have passed through the airport during the screening period. Most cases of illness acquired overseas would probably not have been notifi ed, particularly those in patients with mild illness who did not see a doctor or who saw a doctor but did not receive a diagnosis. The estimated proportion of overseas-acquired cases was based on data from the fi rst 100 cases and would have decreased as the pandemic progressed. The net effect of these factors is unknown, but they would probably have increased the estimated number of undetected infected travelers passing through screening, thereby further reducing the estimated sensitivity of screening.
Border screening might be conducted for reasons other than preventing or delaying an epidemic. It might provide public assurance and confi dence that something is being done (14). The communication of health information and advice on how to seek treatment is consistently recommended as a pandemic prevention strategy (12,15) and is usually delivered as part of border screening programs. These benefi ts need to be balanced against the considerable resources used, opportunity cost (resources used for this activity and thereby unavailable for other activities), uncertain effectiveness, and inconvenience of border screening.
To delay or prevent infl uenza entry at borders, infl uenza screening needs to be considerably more effective than the mostly passive program described here. We hope that during this interepidemic period, a major international review of the role of international air travel in the dissemination of emerging infectious diseases will be conducted to identify effective interventions. Such a review should consider systemwide approaches, including exit screening, standardized health declarations, active screening of individual passengers (including use of rapid laboratory tests and thermal scanning), passenger tracking, policies and practices that support sick travelers wishing to defer travel, and circumstances where airline travel should be suspended entirely.