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, in their belongings, or on their conveyances, 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 21st 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 early part of this century 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 destinations.
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. After a brief hiatus, it reappeared in Vietnam in 2003 and has been in continuous circulation ever since. Even though H5N1 has primarily affected poultry, from 2003 through 2011, 578 human illnesses in 15 countries were reported, with an alarming case-fatality ratio of 59%. The countries with the most human disease (Indonesia, Vietnam, and Egypt) account for 80% of all cases and 78% of all deaths. All 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 influenza A (H1N1)pdm09 [pH1N1], which produced the first pandemic of the 21st century, 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 pH1N1 was identified in that location during the early stages of the pandemic. Aided by travel, this new virus rapidly found its way to dozens of countries after it was identified, resulting in a pandemic designation by the World Health Organization only 2 months later. This virus continues to circulate and has now become a seasonal influenza strain. The pH1N1 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 21st 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, seeding 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 ratified in 2005.
CHILDHOOD VACCINE-PREVENTABLE DISEASES
Vaccination programs have substantially reduced the global prevalence of childhood infectious diseases. In the Western Hemisphere, indigenous measles transmission was declared eliminated in 2000, and diseases like mumps and rubella are at historical lows. Globally, poliomyelitis is on the verge of eradication, and endemic transmission of poliovirus is confined to only 3 countries. However, most vaccine-preventable diseases are highly transmissible and can easily spread in infected travelers. As one example, in recent years, transmission cycles were reestablished because poliovirus was imported into previously polio-free areas.
In the United States, clusters of measles continue to occur as a result of travel. These episodes have been precipitated by visitors from areas of the world where measles continues to circulate because of low vaccination coverage, susceptible US travelers going abroad, and overseas adoptees. These importations then ignite domestic outbreaks because of lower levels of population immunity in some communities, which is fueled largely by parents who elect not to vaccinate their children. In 2011, the United States reported 222 cases of measles, the largest number seen in 15 years. This number contrasts with a median of 56 cases reported per year from 2001 through 2008. Of the 2011 cases, 90% were definitely linked to importation (the remaining 10% were unknown), and 52 cases occurred in US residents exposed while abroad. The leading sources of importation were Europe (46%), Southeast Asia (26%), and the Western Pacific (15%), likely reflective of tourism patterns to and from areas with active measles transmission.
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 6,584 mumps cases being reported across the country. 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 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 central Africa, a large outbreak resulted after introduction of the virus from Angola, producing 441 cases in the Republic of Congo and an additional 104 cases in neighboring Democratic Republic of Congo. In 2011, cases of wild-type polio were identified in 16 countries, although only 1 recognized case occurred in India, which subsequently had no reported cases in more than a year. Although polio does not pose a threat to most travelers, it 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; although an infected traveler is a possibility, importation of infected birds or mosquitoes is considered more likely.
For 2 other major vectorborne infections (dengue and chikungunya), the role of travelers is clear. 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. Since 2000, dengue virus has made incursions into the United States via infected travelers, producing outbreaks with local transmission in Texas, Hawaii (2001, 2011), and Florida (2009–2010, 2011). In Hawaii, for the first time since the 1940s, local dengue transmission was detected in 2001 when an outbreak in Maui resulted in 122 cases. The outbreak source was thought to be travelers from French Polynesia, which was experiencing an outbreak at the time. In 2010, an outbreak was identified in Oahu when 5 locally acquired dengue cases were linked to a sick traveler returning from the Philippines. In 2009, local dengue transmission was seen for the first time in Florida in 6 decades. This resulted in sustained local dengue transmission in 2009 and 2010; 93 cases of dengue were identified, principally among residents of the Florida Keys and tourists to the Florida Keys from other areas of the United States. Although dengue transmission appears to have subsided in the Florida Keys, in 2011 a total of 7 locally acquired infections were identified in 4 other Florida counties. The source of introduction of dengue virus to Florida 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 on 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. This has provided opportunities for local transmission of chikungunya virus to occur, including in 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 that 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.
In October 2010, cholera unexpectedly appeared in Haiti for the first time in recorded history. The cholera outbreak struck in the aftermath of the devastating January 2010 Haiti earthquake, which killed an estimated 316,000 people. The Vibrio cholerae strain (toxigenic serogroup O1, serotype Ogawa, biotype El Tor) responsible for the outbreak did not genetically resemble the Latin American outbreak strain that appeared in the 1990s or strains occasionally found along the coast of the Gulf of Mexico. Instead, it more closely resembled strains recently circulating in south Asia and Africa. A number of hypotheses were advanced regarding how the organism arrived in Haiti, including potential introduction by troops serving as part of the United Nations peacekeeping force housed upstream of the area where the first cases were recognized. Given Haiti’s widespread poverty, poor sanitation, and population displacement in the aftermath of the earthquake, cholera spread rapidly. Shortly after it was recognized, cholera was causing thousands of cases throughout the country per week. As of April 2012, more than half a million cases had been recorded, with almost 300,000 hospitalizations and >7,000 deaths. Cholera subsequently spread to the Dominican Republic, which shares the island of Hispaniola, and Cuba. It also moved via travelers to and from Haiti to other countries, including the United States. Since these other locations have better sanitation infrastructure than Haiti, the risk of local spread of cholera is low. This outbreak provides a dramatic and unfortunate example of how disease can move from place to place with devastating consequences.
Antimicrobial drug resistance among bacteria, viruses, fungi, and parasites is a growing problem. Travelers have frequently aided the spread of drug-resistant pathogens, including drug-resistant strains of Neisseria gonorrhoeae, methicillin-resistant Staphylococcus aureus (MRSA), and multidrug-resistant Acinetobacter baumannii. Highly drug-resistant strains of bacteria that are important causes of health care–associated infection (HAI), for example, carbapenem-resistant Enterobacteriaceae (CRE), have emerged and been spread internationally via travelers. In 2006, HAI outbreaks due to CRE in Israel were linked to a strain common in the United States. More recently, a new and more transferrable drug-resistance mechanism responsible for CRE, known as the New Delhi metallo-β-lactamase-1 (NDM-1), was reported in 2009 in a Swedish citizen of Indian origin who developed medical problems requiring hospitalization while visiting India. After he returned to Sweden, the patient was again hospitalized, and strains of Klebsiella pneumoniae and Escherichia coli that produced NDM-1 were identified. In 2010, NDM-1 was identified in a series of 29 patients in Great Britain; at least 17 of the patients had traveled to the Indian subcontinent in the year before the diagnosis, and 14 of the 17 had been hospitalized during their visits. Similar findings in 3 patients were reported in the United States in 2010. Now, only a few years after the first case in Sweden, NDM-1 is being detected worldwide (Map 1-01), often first being seen in a patient who was previously hospitalized in the Indian subcontinent or the Balkans. This example shows how highly drug-resistant pathogens associated with health care can easily hitchhike from place to place. The growing phenomenon of medical tourism may further accelerate this trend.
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 is an example of how diseases can spread to home countries of returning travelers after an international mass gathering. 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. 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.
Map 1-01. Global spread of New Delhi metallo-β-lactamase-producing Klebsiella pneumoniae, as of June 20121
1Adapted from Figure 4 in: Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis [serial on the Internet]. 2011 Oct [cited 2012 Sep 26]. Available from: http://dx.doi.org/10.3201/eid1710.110655. Additional data provided by Patrice Nordmann.
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