Effect of Travel on Influenza Epidemiology

Sanne-Meike Belderok

, Guus F. Rimmelzwaan, Anneke van den Hoek, and Gerard J.B. Sonder

Author affiliations: Public Health Service, Amsterdam, the Netherlands (S.-M. Belderok, A. van den Hoek, G.J.B. Sonder); Academic Medical Centre, Amsterdam (S.-M. Belderok, A. van den Hoek, G.J.B. Sonder); Erasmus Medical Center, Rotterdam, the Netherlands (G.F. Rimmelzwaan); National Coordination Centre for Traveler’s Health Advice, Amsterdam (G.J.B. Sonder)

Abstract

To assess the attack and incidence rates for influenza virus infections, during October 2006–October 2007 we prospectively studied 1,190 adult short-term travelers from the Netherlands to tropical and subtropical countries. Participants donated blood samples before and after travel and kept a travel diary. The samples were serologically tested for the epidemic strains during the study period. The attack rate for all infections was 7% (86 travelers) and for influenza-like illness (ILI), 0.8%. The incidence rate for all infections was 8.9 per 100 person-months and for ILI, 0.9%. Risk factors for infection were birth in a non-Western country, age 55–64 years, and ILI. In 15 travelers with fever or ILI, influenza virus infection was serologically confirmed; 7 of these travelers were considered contagious or incubating the infection while traveling home. Given the large number of travelers to (sub)tropical countries, travel-related infection most likely contributes to importation and further influenza spread worldwide.

International tourism has increased tremendously, with ≈908 million tourist arrivals at airports worldwide in 2007 (1). The annual number of travelers from the Netherlands to tropical and subtropical countries, in a population of ≈16 million persons, doubled from ≈1 million in 1999 to ≈2 million in 2007 (2). Increased health risks, particularly infectious diseases, are associated with travel. Prospective studies estimate that up to 64% of short-term travelers experience an illness related to travel to (sub)tropical countries (3–5). In these studies, respiratory tract infections were the second most frequent infectious disease contracted during travel, with attack rates (ARs) up to 26%; fever affected 11%–19.9% of travelers while they were abroad (3–6). Influenza is one of the most frequently acquired infectious diseases among travelers (7). Respiratory tract infections, including influenza in 6% of cases, commonly caused illness among patients admitted to a tertiary-care hospital after they returned from travel (8). Among febrile travelers examined at hospitals after return, influenza was diagnosed in up to 15% (9–11).
The World Health Organization (WHO) estimates that ≈5%–15% of the worldwide population is affected by seasonal influenza viruses annually (3). Outbreaks of influenza associated with travel by air, ship, or train indicate that international travelers are at risk for this infection (12–14) and may introduce novel strains into domestic populations (15,16). Indeed, in Europe in 2009, >29% of all confirmed cases of influenza A(H1N1)pdm09 virus were related to travel (17). Also, of patients admitted to Tan Tock Seng Hospital in Singapore with confirmed influenza A(H1N1) infection, 25% had traveled by plane after onset of illness, and 15% became ill while traveling (18).
The incubation period for influenza is 1–5 days, with adults most infectious from 1 day before symptom onset to ≈5–7 days after symptom onset. In healthy adults, a wide range of symptoms occur, varying from classic influenza and mild illness to asymptomatic infection (19). Because influenza is highly contagious and has a short incubation period, travel probably contributes considerably to the rapid spread of the virus (20).
In temperate climates, influenza is seasonal: most influenza activity occurs in winter, in the Northern Hemisphere during November–March and in the Southern Hemisphere during April–October. In the tropics, however, the destination of many short-term travelers, influenza virus circulates at low levels year-round (21,22).
Prospective research on influenza during travel is sparse. To our knowledge, the only prospective study that estimated the AR and incidence rate (IR) of influenza among travelers was a cohort study conducted during 1998–2000 (6). This study reported that 1.2% of all travelers had a confirmed influenza virus infection, defined as a >4-fold increase in antibody titers, and an influenza incidence of 1.0 per 100 person-months abroad. We prospectively estimated the AR and IR for influenza, risk factors for and proportion of symptomatic and asymptomatic travelers, and geographic areas with particular risk.