Perspectives: The Role of the Traveler in Translocation of Disease
Since humans began moving from one place to another, they have offered free passage to pathogens, on themselves or in their belongings, and the consequences of such microbial hitchhiking have, at times, altered the course of history. Among the more notable examples are the great plagues that swept into Europe from Asia during the Middle Ages, the importation of smallpox to the Americas by European explorers, and the reverse movement of syphilis into Europe in those same returning explorers.
Although the movement of pathogens through travel is not a new phenomenon, today’s increasing pace and scale of global human movement have enhanced the opportunities for disease spread. HIV infection, with symptoms that may be delayed for years, spread around the world less than a decade after it was recognized. In the twenty-first century, no place on the globe is more than a day from any other location, which gives even diseases with short incubation periods unprecedented opportunities for rapid spread. The following examples from the last decade illustrate the role travel plays in the translocation of infectious diseases. They also remind us that all travelers should take steps to prevent bringing more than luggage to their destination.
Two new forms of influenza have recently emerged. One is avian influenza A (H5N1), which was first observed during a limited-scale outbreak in Hong Kong in 1997. It reappeared in Vietnam in 2003 and has been in continuous circulation ever since. Even though H5N1 has primarily affected poultry, from 2003 through 2009, 458 human illnesses in 15 countries were reported, with an alarming case-fatality ratio of 62%. The countries with the most human disease (Indonesia, Vietnam, and Egypt) are tourist destinations, but no international travelers have become ill, largely because close contact with infected poultry is the primary risk factor for infection, and no sustained human-to-human transmission has been observed. However, movement of the virus between countries in goods carried by conveyances and animals has been documented.
In contrast, the rapid spread of 2009 pandemic influenza A (H1N1) was aided by infected travelers, both those who were symptomatic and those who were in the incubation stage. Although the virus was first identified in southern California in April 2009, human illnesses appeared weeks earlier in Mexico. Infected travelers who had visited Mexico were quickly detected in other parts of the world. An analysis of air traffic patterns found a very strong correlation between the volume of air travel from Mexico to a country and the likelihood H1N1 was identified in that location during the early stages of the pandemic. Aided by travel, this new virus found its way to dozens of countries in less than 2 months after it was identified, resulting in a June 2009 pandemic designation by the World Health Organization. The H1N1 pandemic vividly demonstrates the potential for global dissemination of pathogens in a highly interconnected world.
The severe acute respiratory syndrome (SARS) epidemic of 2003 is another major example of the role of travel in the spread of infectious diseases in the twenty-first century. In February 2003, a professor from southern China, who was caring for patients with an unrecognized respiratory illness, traveled to a family wedding in Hong Kong while he was ill. His infection spread to 10 other travelers in his hotel, who then boarded airplanes to other parts of Asia, North America, and Europe, setting off a global epidemic of SARS that resulted in 8,098 cases and 774 deaths in 29 countries. Fortunately, characteristics of the virus, transmission dynamics of the disease, and aggressive public health measures contained the virus within months, but not before SARS produced widespread fear, and economic and political turmoil. SARS had a major influence on the revisions to the International Health Regulations in 2005.
CHILDHOOD VACCINE-PREVENTABLE DISEASES
Vaccination programs have substantially reduced the global prevalence of childhood infectious diseases. In the Western Hemisphere, measles transmission has been effectively eliminated, and diseases like mumps and rubella are at historical lows. Globally, poliomyelitis has been targeted for eradication, and by the early 2000s, transmission of indigenous poliovirus was confined to only 4 countries. However, these diseases are all highly transmissible and can easily spread in infected travelers; endemic transmission has been reestablished in some previously polio-free areas.
In the United States, all recent clusters of measles have been associated with travel. These episodes have been precipitated by visitors from areas of the world where measles continues to circulate due to low vaccination coverage, susceptible US travelers going abroad, and overseas adoptees. These importations then ignite outbreaks because of waning population immunity, which is fueled largely by parents who elect not to vaccinate their children. During the first half of 2008, 13% of measles cases with an identified source were imported, and 76% of the remaining cases were the result of subsequent local transmission. In the previous decade, 20%–60% of cases were imported, and subsequent spread was much more limited.
Several recent large outbreaks of mumps in the United States are directly traceable to travel-related importation from Great Britain. A 2006 outbreak centered in Iowa, likely fueled by spring break travel, resulted in more than 2,500 cases across 11 states. A more recent outbreak that began in mid-2009, resulting in more than 2,000 cases in New York City and surrounding states, largely centered around an Orthodox Jewish community. This outbreak was started by a single traveler to Great Britain who returned to a summer camp in New York State. Mumps then spread to campers and staff, who carried it home to New York City and ignited sustained transmission for many months.
In 2002, only 6 countries had circulating indigenous wild-type poliovirus, but from 2002 through 2007, wild-type poliovirus spread to 27 previously disease-free countries in Africa and Asia through the movement of infected travelers. Northern Nigeria was the source of most of these illnesses, which reached all the way to Indonesia. Vaccination campaigns, guided by laboratory-based surveillance, largely disrupted transmission in these places, but travel continues to result in the spread of polio. In 2008–2009, there were 47 introductions or reintroductions of the virus into 17 African countries, all originating from Nigeria or India, resulting in 255 subsequent cases. In 2010, even as polio incidence decreased in Nigeria and India, 2 large outbreaks demonstrated the risk of introduction from poliovirus reservoirs. Spread of poliovirus into Tajikistan from India caused an outbreak of 458 cases and, subsequently, 18 cases in 2 other Central Asian republics and Russia. In the Republic of the Congo, a large outbreak (more than 300 suspected cases as of late November 2010) resulted after introduction from Angola, posing further risk of spread elsewhere. Although these cases do not threaten most travelers, polio remains a serious concern for migrants, pilgrims, and people displaced by conflict; outbreaks heavily tax the public health resources of affected countries.
Several mosquito-transmitted diseases have expanded their range in the last decade. West Nile virus was introduced into New York City in 1999 and, in the next several years, spread throughout the Western Hemisphere, resulting in millions of human infections. The source and mode of introduction are unknown; an infected traveler is a distinct possibility, although importation of infected birds or mosquitoes is considered more likely.
For 2 other major vectorborne infections (dengue and chikungunya), the role of travelers is much clearer. Neither of these viruses has an avian intermediary, and humans are amplifying hosts for both viruses, effectively moving these viruses from place to place. Dengue outbreaks are expanding in scale and scope, especially in Asia and South America. Twice since 2000, the virus has made incursions into the United States via infected travelers. In 2001, local transmission was detected on Maui in Hawaii for the first time since the 1940s, resulting in 122 cases. The source was travelers from French Polynesia, which was experiencing an outbreak at the time. In 2009–2010, local dengue transmission was seen in the Florida Keys, also for the first time in decades. More than 70 cases were identified, including in tourists to the Florida Keys from other areas of the United States. The source of introduction is unknown, although many people from areas where dengue is endemic transit through the area.
Chikungunya virus was largely restricted to Africa and Asia until it began to appear in islands of the Indian Ocean in 2005, after an outbreak in Kenya in 2004. From there, it crossed to the Indian subcontinent in 2006, touching off major disease outbreaks, especially in southern India. Sizeable numbers of travelers to Indian Ocean tourist destinations and India have returned to Europe, North America, and Australia infected with chikungunya virus, and infected Indian nationals have also been seen in these locations. Chikungunya virus can be introduced into these areas in the same way that West Nile virus was introduced into the United States in 1999. Such events have taken place in several areas, including northern Italy in 2007, and southeast France and south-central China in 2010. The source for translocation in Italy was a viremic traveler from India. A total of 205 locally acquired cases were acquired through infected Aedes albopictus mosquitoes, an invasive species which appeared in the area in the early 1990s. In contrast to West Nile in North America, chikungunya virus does not appear to have persisted in northern Italy. Many countries that have a viable vector for chikungunya virus remain at risk for importation and local transmission. Map 1-01 shows the general pattern of how the chikungunya virus spread globally during these years.
DISEASE ASSOCIATED WITH GLOBAL GATHERINGS
The pilgrimage to Mecca is the world’s largest annual event, drawing approximately 2 million Muslims from across the globe to Saudi Arabia. The history of the Hajj pilgrimage serves as an example of how diseases can spread during a global mass gathering, and can spread to home countries of returning travelers. The intermingling and close contact offer ample opportunities for transmission of infectious diseases and rapid dissemination as pilgrims return home. In 2000, this occurred with Neisseria meningitidis serogroup W-135, despite requirements for pilgrims to be vaccinated against meningococcal disease. Some vaccines used at that time did not cover this serogroup. After the event, 90 infections in returnees and their contacts were seen across Europe. In contrast, the number of infections in North America, where quadrivalent vaccine that covered W-135 was in use, was small. The outbreak strain of W-135 also quickly surfaced across areas of Africa, Asia, the Middle East, and the Indian Ocean, altering the epidemiologic patterns of meningococcal disease. As a result of this outbreak and similar cases in 2001, pilgrims to the Hajj are now required to be vaccinated with the quadrivalent vaccine.
These examples highlight the diversity of opportunities for microbial movement afforded by travel. No amount of vigilance is likely to eliminate such opportunities, especially since microbes can be silent travelers. However, all travelers should take precautions to prevent the spread of disease.
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