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Population Movements and Emerging Diseases
Mary E. Wilson
We are a world in motion. In 1996,2.5 billion people passed through airports. Travel today is unprecedented
in its speed, volume, and reach. N o environment is too
harsh and no destination too distant to discourage exploration. But much of the movement of populations today
is unplanned and unwelcome, a consequence of environmental, economic, or political pressures.
This brief paper will make four main points:
individual by about one order of magnitude. Travel for
the individual increased by a factor of more than 1000
during this time period. Figure 1 shows the exponential growth in daily travel range since 1800. Recent
trends would bear this out.Air traffic volume has increased
about 7% per year for the past 20 years.’ About 5000 airports have scheduled worldwide service. More than 500
million persons cross international borders on commercial flights each year.
A greater range of travel means potential exposure
to a larger variety of species, some of which may cause
harm to us.’ Exploration and development of new lands
may involve entry into new habitats and contact with
microbes in soil and aninials not previously recognized
as human pathogens. An example is the recent recognition of a form of hemorrhagic fever (Venezuelan hemorrhagic fever) caused by a newly characterized arenavirus
(Guanarito ~ i r u s )When
.~
we travel, we are both recipients and dispersers of microbes.We may complete a loop
by picking~.
up microbial flora in a new land and carrying it honie to friends and family, perhaps sharing it along
the way with fellow travelers. A large outbreak of
antibiotic-resistant shigellosis involving niore than 50%
of the estimated 12,700 persons at a mass gathering in
North Carolina was followed by the nationwide dissenlination of the organism and outbreaks in at least three
other states.’
’
Movement involves all biologic species; movement
of nonhuman species is also relevant to hunian
health.
Migrating humans, while at risk for new infections,
also aid in the global dispersal of infections.
Human activities provide increased opportunities for
genetic exchange among microbes and favor the
selection and spread of resistant strains.
Population
growth, increasing urbanization, and
(4)
environmental change enhance the emergence and
spread of infections.
Travel continues to increase. In a book called The
Rise and Fall oflnjrastructures, Grubler’ analyzed the average kilometers traveled daily per capita in France, starting with the year 1800 and continuing through the
present. H e included horses, railways, buses, cars, and air
travel, among others. What is notable is that each new
transportation mode increased the average range of an
Mary E. Wilson, MD:Assistant Professor, Departments of
Population and International Health and Epidemiology,
Harvard School of Public Health, Boston, Massachusetts;
Assistant Clinical Professor, Harvard Medical School, Boston,
Massachusetts; and Chief of Infectious Diseases and
Director,Travel Resource Center, Mount Auburn Hospital,
Cambridge, Massachusetts.
lo.m
1.m
This paper was presented in part at the Harvard School of
Public Health 75th Anniversary Symposium, Gateway to
World Health: New Science and Strategies in Public Health,
1997.
IW
I0
I
Reprint requests: Mary E. Wilson, MD, Mount Auburn
Hospital, 330 Mount Auburn Street, Cambridge, MA 02238,
USA.
Figure 1 Range covered (average km traveled daily) per
capita in France by mode and total since 1800. Source: Grubler?
JTravel Med 1997; 4:183-186.
Reprinted with permission.
183
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A century and a half ago,John Snow recognized the
importance of travel and trade in the spread of cholera.
H e noted:"Epidemics of cholera follow major routes of
commerce. The disease always appears first at seaports
when extending into islands or continents.""The role of
travel and trade today persists and is expanding.
We cannot talk about population movements without noting the massive population shifts that occur as a
consequence of social and political unrest, economic
and environmental pressures, and war.',' In the early
1990s, there were an estimated 20 million refugees and
30 million displaced persons.' Extreme weather events,
such as floods, hurricanes, and droughts, displace persons
from their homes. These semi to be occurring with
increased frequency and have a growing impact as more
people settle in coastal and vulnerable regions."'
Population displacements are accompanied by conditions that favor disease emergence and spread.Witness
the massive outbreaks of cholera, dysentery, measles, and
other infectious diseases in refugee camps." In the late
1980s, hundreds of cases of visceral leishmaniasis were
diagnosed in Khartoum among migrants to that area who
had been displaced from their homeland by war and
famine. Malnutrition and nomadic movement of populations into areas endemic for leishinaniasis were contributing factors in the outbreak."
We are not the only species moving about the earth.
When we travel, we carry our microbial flora in and on
our bodies. HIV has spread throughout the world, transported by the human host.13We carry the microbes that
cause tuberculosis, influenza, shigellosis, pneuniococcal
pneumonia,14staphylococcal infections," and also microbial genetic material that through transfer, recombination, conjugation, reassortment and a variety of molecular
maneuvers can confer virulence or resistance to other
microbes."
We also facilitate the dispersal of other species
through shipping and commerce." We transport food,
animals, insects, plants, seeds, and other materials about
the globe on boats, planes, trucks, and trains.'>l8We have
given wings to species that were previously confined to
one geographic region. Our transport systems vastly
amplie and extend the natural biologic movement of
other species that has always occurred through migration, winds, ocean currents, and streams.
Even if we do not travel, pathogens have multiple
routes available to reach us.The globalization of markets
nieans that fruits and vegetables harvested in one area may
be consumed thousands of miles away." Alfalfa sprouts
grown from contaminated seed sent to a Dutch shipper
caused outbreaks of salmonella infections on two continents, in at least Arizona and Michigan in the United
States and in Finland.'"The food chain has become very
long.As it stretches around the globe, we have added new
J o u r n a l o f T r a v e l M e d i c i n e , V o l u m e 4, N u m b e r 4
links.Analysis of another outbreak of salmonellosis identified a complex route that included wild animals, farm
animals, animal feed, slaughterhouses, processing plants,
retail outlets, and finally the human consumer.21
Old, familiar pathogens can enierge to cause new
problems if they enter new populations, become resistant to drugs used to treat them, or if virulent clones
emerge. Increasingly, Streptococcus pneumoniae is becoming resistant to penicillin and other commonly available
antimicrobials. A group C, ET-15 strain of Neisseria
rneningitidis, which was more virulent than were previous strains, spread in Canada and was associated with an
increased case fatality rate and a higher proportion of cases
in persons over the age of five."
Commercial movement of fruits and vegetables
redistributes resistance factors along with the microbes.
In addition, antibiotics used in aquafarnling are the same
ones used to treat human infections, and antibiotics used
in farmed fish reach wild fish in nearby ponds. In one
study,74-100% ofwild fish in close proximity to treated
ponds had residues of quinolones."
Bacteria have an impressive array of ways to acquire
resistance.Many genes that determine resistance predate
the use of antimicrobials. It now appears clear that horizontal as well as vertical transfer of resistance genes is
common in the niicrobial kingdom. Bacteria can take up
foreign DNA and incorporate it into their chromosomes. Resistance to multiple antibiotics can be transferred together. Bacteria can spread resistance to unrelated
bacteria. Today we are providing bacteria more opportunities for genetic exchange through access to more populations; at the same time, broad use of antimicrobials
applies selective pressure that favors survival of resistant
organisms."
Molecular markers make it possible to trace the
spread of specific microbes. Pilgrims carried an epidemic strain of group A Neisseria meningitidis from southern Asia to Mecca in 1987.Other pilgrims who became
colonized with the epidenlic strain introduced it into subSaharan Africa, where it caused a wave of epidemics in
1988 and 1989.'4 Multidrug-resistant strains of Streptococcus pneumoniac were introduced into Iceland.2s Many
examples exist of the global spread of multidrug-resistant strains o r virulent strains of common human
pathogens. Using molecular techniques coupled with epidemiologic data, investigators were able to show the
emergence of multidrug-resistant tuberculosis clones in
NewYork, and their dissemination in NewYork City and
to at least four additional cities in the United States."
Movement of insect species can also affect hunian
health. In March 1930 in Brazil an entomologist on a Sunday stroll came upon Anopheles garnbiae larvae, to his
great surprise." The usual habitat of this mosquito was
Afiica.The postulated route of entry into South America
Wilson, Population Movements and Emerging Diseases
was on boats that made mail runs between Dakar, Senegal, and Natal, Brazil, covering the 3300 km in less than
100 hours. Over the ensuing years, the mosquito spread
along the coastal region and moved inland, often traveling on river boats. In 1938 and 1939 there were devastating outbreaks of malaria that caused more than
20,000 deaths. Although malaria already existed in the
area, the local mosquitoes were not efficient vectors. In
contrast, the new mosquito, Anopheles gambiae, lived in
close proximity to humans, entered houses, sought human
blood, and was an efficient biter. In this case the simple
introduction of a new mosquito vector caused severe
problems. Fortunately, an intensive eradication campaign
was effective."
This event in Brazil is not just a historic anomaly.
We regularly transport vectors around the globe. Aedes
albopictcrs was introduced into the United States in used
tires shipped from Asia and has since spread to at least
21 contiguous states and H a ~ a i i . ~This
~ - ~ mosquito
"
transmits dengue in Asia and is a competent laboratory
vector for a number of human pathogens, including yellow fever, La Crosse, and other viruses.
Insects are hardy creatures.When mosquitoes, houseflies, and beetles in special cages were placed in wheel
bays of 747 aircraft and carried along on flights lasting
up to 7 hours, they survived despite outside temperatures
as low as -52°C.Temperatures in the wheel bays ranged
from 8-25OC. More than 99% of the beetles, 84% of the
mosquitoes, and 93% of the flies survived the trip.3' We
occasionally see human disease as a direct result of these
mosquito flights, so-called airport malaria: cases of malaria
near airports in temperate regions, presumably from jetsetting mosquitoes that survived long enough in the
new environment to take at least one blood meal?
Introductions of species, whether microbes, plants,
or animals, into new regions can have profound effects
on local ecosystems.What is changing is the frequency
with which invasions are occurring. Since 3 960, more
than 40 new species have appeared in the Great Lakes;
since 1970, more than 50 have appeared in San Francisco
Bay?
Most people think of a boat as a form of transportation, but it is also a floating biological island. In addition to passengers, crew, and cargo, ships transport
biologic life around the globe in ballast, on the hull and
in ship chests.Today 80% of the world trade volume is
transported by ship. The increasing speed of travel
increases the probability of the survival of species carried by sea. Ballast water, necessary to maintain the stability of ships, is taken on in one or multiple sites,
transported, and discharged at another time and place.
The volume is huge. In a large tanker, for example, the
volume of ballast may exceed 200,000 cubic meters. It
is a rich biological soup, containing viruses,bacteria, fungi
185
and basically all plants and animals less than 1 cm in size
that happen to be adjacent to the boat at the time ballast water is taken in. It has been estimated that ballast
water transports more than 3000 species around the
world each day." In Coos Bay, Oregon, researchers
studied ballast water from 159 cargo ships that had
come from 25 Japanese ports.They were able to identify a minimum of 367 different t a ~ a ? ~
We can also note potential threats to human health
related to release ofballast water. In studies ofballast and
bilge of cargo ships in the U.S. Gulf of Mexico, researchers
were able to identify Vibrio cholerae identical to the strains
causing epidemic disease in Latin A m e r i ~ a . ~ '
In most instances, the emergence of an infection
involves multiple factors often interacting in complex
ways. For example, dengue fever, a viral infection spread
by mosquitoes, has exploded in Latin America in the
1990~.~~Traveling
humans have introduced the virus, but
other conditions have helped it flourish. Aedes aegypti, an
effective vector, has reinfested many areas.Widespread use
of nonbiodegradable plastic containers provides good
breeding conditions for the mosquito. Increasing urbanization, especially in tropical zones, means that more
urban areas will reach the critical population size, perhaps somewhere between 150,000 and 1 million, to
permit endemic transmission and to increase the risk of
the severe forms of infection: dengue hemorrhagic fever
and dengue shock ~yndrome.~'
Recent studies suggest
other reasons for concern. Over the past two centuries
the number of dengue lineages has been increasing
roughly in parallel with the increasing size of the human
p~pulation.~~Will
an expanding human population allow
increasing rates of viral evolution and enhance the potential for the appearance of more virulent strains?
Conclusions
In summary, a few points bear emphasis. Global
movement is massive, involves all species, and can be
expected to expand in volume, speed and reach in the
foreseeable future. Distributions of species are changing
at an unprecedented rate. New juxtapositions of species
allow exchange of genetic information that can affect
human health through direct and indirect mechanisms.
Population size and density can influence the spread
and evolution of infectious diseases.
Global movement of populations and evolution of
microbes will continue and will present an ongoing
challenge for practitioners of travel medicine. New infections will continue to emerge, and known infections will
change in distribution, severity, and frequency. In today's
world, socioeconomic, political, environmental, and
demographic changes have converged to allow many
infectious diseases to flourish. Any meaningful response
186
must integrate knowledge and skills from social, biological, and physical sciences and approach the problem at
a systems level. Enhanced global surveillance and communication are essential to provide care for individual
patients and to respond to outbreaks.
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