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Emerging Vol. 1, No. 2, April–June 1995 Infectious Diseases Travel and the Emergence of Infectious Diseases Mary E. Wilson Escherichia coli Serotype O157:H7 Peter Feng Epidemic-Associated Neisseria meningitidis Michael W. Reeves Dengue/Dengue Duane J. Gubler and Hemorrhagic Fever Gary G. Clark Eradication of Dracunculiasis Ernesto Ruiz-Tiben Escherichia coli O169:H41 in Japan Yoshikazu Nishikawa The GAP Project in Southeastern Turkey Serap Aksoy Drug-Resistant Streptococcus pneumoniae Martin S. Cetron WHONET: Monitoring Thomas F. O’Brien and Antimicrobial Resistance John M. Stelling Preventing the Spread of Hospital Infection Control Vancomycin Resistance Practices Advisory Committee Waterborne Cryptosporidiosis Daniel G. Colley U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES Public Health Service Emerging Infectious Diseases Editors Liaison Representatives Editor Anthony I. Adams, M.D. Joseph Losos, M.D. Joseph E. McDade, Ph.D. Chief Medical Adviser Director General National Center for Infectious Diseases Commonwealth Department of Laboratory Center for Disease Control Centers for Disease Control Human Services and Health Ontario, Canada and Prevention (CDC) Canberra, Australia Atlanta, Georgia, USA Gerald L. Mandell, M.D. David Brandling-Bennett, M.D. Liaison to Infectious Diseases Society Perspectives Editor Deputy Director of America Stephen S. Morse, Ph.D. Pan American Health Organization University of Virginia Medical Center The Rockefeller University World Health Organization Charlottesville, Virginia, USA New York, New York, USA Washington, D.C., USA Robert Shope, M.D. Synopses Editor Gail Cassell, Ph.D. Director, Yale Arbovirus Research Unit Phillip J. Baker, Ph.D. Liaison to American Society for Yale University School of Medicine Division of Microbiology and Microbiology New Haven, Connecticut, USA Infectious Diseases University of Alabama at Birmingham National Institute of Allergy and Birmingham, Alabama, USA Bonnie Smoak, M.D. Infectious Diseases Chief, Dept of Epidemiology National Institutes of Health (NIH) Richard A. Goodman, M.D., M.P.H. Division of Preventive Medicine Bethesda, Maryland, USA Editor, MMWR Walter Reed Army Institute of Research Centers for Disease Control Washington, D.C., USA Dispatches Editor and Prevention (CDC) Stephen Ostroff, M.D. Atlanta, Georgia, USA Robert Swanepoel, B.V.Sc., Ph.D. National Center for Infectious Diseases Head, Special Pathogens Unit Centers for Disease Control William Hueston, D.V.M., Ph.D National Institute for Virology and Prevention (CDC) Acting Leader, Center for Animal Sandrinham 2131, South Africa Atlanta, Georgia, USA Health Monitoring Centers for Epidemiology and Roberto Tapia, M.D. Managing Editor Animal Health Director General de Epidemiología Polyxeni Potter, M.A. Veterinary Services, Animal and Plant Dirección General de Epidemiología National Center for Infectious Diseases Health Inspection Service Secretaría de Salud Centers for Disease Control U.S. Department of Agriculture México and Prevention (CDC) Fort Collins, Colorado, USA Atlanta, Georgia, USA Morag Timbury, M.D. James LeDuc, Ph.D. Director Advisor for Arboviral Diseases Central Public Health Laboratory Division of Communicable Diseases London, United Kingdom Editorial and Computer Support World Health Organization Emerging Infectious Diseases receives Geneva, Switzerland editorial and computer support from the Office of Planning and Health Communication, National Center for Infectious Diseases. Emerging Infectious Diseases Editorial Support Maria T. Brito Emerging Infectious Diseases is published four times a year by the National Center for Beatrice T. Divine, M.B.A. Infectious Diseases, Centers for Disease Control and Prevention (CDC), 1600 Clifton Sharon D. Hoskins Road., Mailstop C-12, Atlanta, GA 30333, USA. Telephone 404-639-3967, fax Anne D. Mather 404-639-3039, e-mail [email protected]. Carol D. Snarey, M.A. The opinions expressed by authors contributing to this journal do not necessarily Production reflect the opinions of CDC or the institutions with which the authors are affiliated. Beverly J. Holland All material published in Emerging Infectious Diseases is in the public domain and may be used and reprinted without special permission; proper citation, however, is Electronic Distribution appreciated. Carol Y. Crawford Wendell Ramirez Use of trade names is for identification only and does not imply endorsement by the Cheryl G. Shapiro, M.S. Public Health Service or by the U.S. Department of Health and Human Services. Editorial Policy and Call for Articles The goals of Emerging Infectious Diseases (EID) are to promote the recognition of new and reemerging infectious diseases and to improve the understanding of factors involved in disease emergence, prevention, and elimination. EID has an international scope and is intended for professionals in infectious diseases and related sciences. We welcome contributions from infectious disease specialists in academia, industry, clinical practice, and public health as well as from specialists in economics, demography, sociology, and other disciplines whose study elucidates the factors influencing the emergence of infectious diseases. EID will be published in English and will feature three types of articles: Perspectives, Synopses, and Dispatches. The purpose and requirements of each type of article are described in detail below. Instructions to Authors Editorial Material: Manuscripts should be prepared to reviews of new and emerging diseases; however, timely according to the “Uniform Requirements for Manuscripts updates of other diseases or topics are also welcome. Submitted to Biomedical Journals” (JAMA 1993:269[17]: Synopses should be approximately 3,500 words and 2282-6). should include references, not to exceed 40. The section should begin with an introduction outlining the Begin each of the following sections on a new page and in this order: title page, abstract, text, acknowledgments, relationship of the issues discussed in the paper to the emergence of infectious diseases. Use of additional references, each table, figure legends, and figures. On the title page, give complete information about each author subheadings in the main body of the text is recommended. If detailed methods are included, a (full names and highest degree). 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If detailed methods are included, a Submit photographs in camera-ready hardcopy. separate section on experimental procedures should Send all manuscripts and correspondence to the immediately follow the body of the text. Photographs and Editor, Emerging Infectious Diseases, National Center for illustrations are optional. Provide a short abstract (150 Infectious Diseases, Centers for Disease Control and words) and a brief biographical sketch. Prevention, 1600 Clifton Road, Mailstop C-12, Atlanta, Synopses: Submit concise reviews of infectious GA 30333, USA, or by e-mail on the Internet to diseases or closely related topics. Preference will be given [email protected]. Contents Emerging Infectious Diseases Volume 1 • Number 2 April–June 1995 Perspective Travel and the Emergence of Infectious Diseases 39 Mary E. Wilson Synopsis Escherichia coli Serotype O157:H7: Novel Vehicles of Infection and 47 Peter Feng Emergence of Phenotypic Variants Dispatches Epidemic-Associated Neisseria meningitidis Detected by Multilocus 53 Michael W. Reeves, Bradley A. Enzyme Electrophoresis Perkins, Marion Diermayer, and Jay D. Wenger Dengue/Dengue Hemorrhagic Fever: 55 Duane J. Gubler and Gary G. Clark The Emergence of a Global Health Problem Progress Toward the Eradication of Dracunculiasis 58 Ernesto Ruiz-Tiben, Donald R. (Guinea Worm Disease): 1994 Hopkins, Trenton K. Ruebush, and Robert L. Kaiser Letters Heat-Stable Enterotoxin-Producing Escherichia coli O169:H41 in Japan 61 Yoshikazu Nishikawa, Masaki Hanaoka, Jun Ogasawara, Nelson P. Moyer, and Teruo Kimura The GAP Project in Southeastern Turkey: The Potential for Emergence 62 Serap Aksoy, Sedat Ariturk, of Diseases Martine Y. X. Armstrong, K. P. Chang, Zeynep Dörtbudak, Michael Gottlieb, M. Ali Ozcel, Frank F. Richards, and Karl Western Commentary Action Plan for Drug-Resistant Streptococcus pneumoniae 64 Martin S. Cetron, Daniel B. Jernigan, Robert F. Breiman, and the DRSP Working Group News and Notes WHONET: An Information System for Monitoring Antimicrobial 66 Thomas F. O’Brien and John M. Resistance Stelling Recommendations for Preventing the Spread of Vancomycin Resistance 66 Hospital Infection Control Practices Advisory Committee Waterborne Cryptosporidiosis Threat Addressed 67 Daniel G. Colley Electronic Access to Emerging Infectious Diseases If you have Internet access, you can retrieve the pub/EID directory in each of the file types listed free Adobe Acrobat Reader by subscribing to the list. journal electronically through file transfer protocol above. EID-PS sends the journal in PostScript format. How- (FTP), electronic mail, or World-Wide Web (WWW). 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You can get the Perspective Travel and the Emergence of Infectious Diseases Mary E. Wilson, M.D. Harvard School of Public Health and Harvard Medical School, Boston, Massachusetts, USA Member: Harvard Working Group on New and Resurgent Infectious Diseases Travel is a potent force in the emergence of disease. Migration of humans has been the pathway for disseminating infectious diseases throughout recorded history and will continue to shape the emergence, frequency, and spread of infections in geographic areas and populations. The current volume, speed, and reach of travel are unprece- dented. The consequences of travel extend beyond the traveler to the population visited and the ecosystem. When they travel, humans carry their genetic makeup, immu- nologic sequelae of past infections, cultural preferences, customs, and behavioral patterns. Microbes, animals, and other biologic life also accompany them. Today’s massive movement of humans and materials sets the stage for mixing diverse genetic pools at rates and in combinations previously unknown. Concomitant changes in the environment, climate, technology, land use, human behavior, and demographics converge to favor the emergence of infectious diseases caused by a broad range of organisms in humans, as well as in plants and animals. Many factors contribute to the emergence of in- survive, proliferate, and find a way to enter a sus- fectious diseases. Those frequently identified in- ceptible host. Any analysis of emergence must look clude microbial adaptation and change, human at a dynamic process, a sequence of events, a milieu, demographics and behavior, environmental or ecosystem. changes, technology and economic development, Movement, changing patterns of resistance and breakdown in public health measures and surveil- vulnerability, and the emergence of infectious dis- lance, and international travel and commerce (1-4). eases also affect plants, animals, and insect vectors. This paper will examine the pivotal role of global travel and movement of biologic life in the emer- gence of infectious diseases. It will also examine the Table 1. Basic concepts in disease ways in which travel and movement are inextricably emergence* tied at multiple levels to other processes that influ- ence the emergence of disease. Emergence of infectious diseases is complex. Travel is a potent force in disease emergence and Infectious diseases are dynamic. spread (5). The current volume, speed, and reach of Most new infections are not caused by genuinely travel are unprecedented. The consequences of mi- new pathogens. gration extend beyond the traveler to the population visited and the ecosystem (6). Travel and trade set Agents involved in new and reemergent the stage for mixing diverse genetic pools at rates infections cross taxonomic lines to include and in combinations previously unknown. Massive viruses, bacteria, fungi, protozoa, and helminths. movement and other concomitant changes in social, The concept of the microbe as the cause of disease political, climatic, environmental, and technologic is inadequate and incomplete. factors converge to favor the emergence of infectious Human activities are the most potent factors diseases. driving disease emergence. Disease emergence is complex. Often several Social, economic, political, climatic, technologic, events must occur simultaneously or sequentially and environmental factors shape disease for a disease to emerge or reemerge (Table 1) (6). patterns and influence emergence. Travel allows a potentially pathogenic microbe to be introduced into a new geographic area; however, to Understanding and responding to disease be established and cause disease a microbe must emergence require a global perspective, conceptually and geographically. Address for correspondence: Mary E. Wilson, Division of The current global situation favors disease Infectious Diseases, Mt. Auburn Hospital, 330 Mt. Auburn emergence. Street, Cambridge, MA 02238 USA, fax 617-965-6632; e-mail [email protected]. *Adapted from Wilson ME (6). 39 Vol. 1, No. 2 — April-June 1995 Emerging Infectious Diseases Perspective Analysis of these species can hold important lessons tients remained infectious for about 3 weeks, many about the dynamics of human disease. opportunities for transmission were available. Even To assess the impact of travel on disease emer- in this century, until the 1970s, smallpox continued gence, it is necessary to consider the receptivity of a to cause epidemics. A pilgrim returning from Mecca geographic area and its population to microbial in- was the source of a large outbreak in Yugoslavia in troduction. Most introductions do not lead to dis- the early 1970s that resulted in 174 Yugoslav cases ease. Organisms that survive primarily or entirely and 35 deaths (9). The pilgrim apparently con- in the human host and are spread through sexual tracted the infection in Baghdad while visiting a contact, droplet nuclei, and close physical contact religious site. Because his symptoms were mild, he can be readily carried to any part of the world. For was never confined to bed and was able to continue example, AIDS, tuberculosis, measles, pertussis, his travels and return home. diphtheria, and hepatitis B are easily carried by For most of history, human populations were rela- travelers and can spread in a new geographic area; tively isolated. Only in recent centuries has there however, populations protected by vaccines resist been extensive contact between the flora and fauna introduction. Organisms that have animal hosts, of the Old and New Worlds. Schoolchildren hear the environmental limitations, arthropod vectors, or rhyme “Columbus sailed the ocean blue, in fourteen complicated life cycles become successively more hundred ninety-two,” but may learn little about the difficult to “transplant” to another geographic area disaster brought upon the native populations of the or population. Epidemics of dengue fever and yellow Americas by the arriving explorers. By the end of the fever cannot appear in a geographic area unless fifteenth century, measles, influenza, mumps, small- competent mosquito vectors are present. Schis- pox, tuberculosis, and other infections had become tosomiasis cannot spread in an environment unless common in Europe. Explorers from the crowded a suitable snail intermediate host exists in that urban centers of Europe brought infectious diseases region. Organisms that survive only under carefully to the New World (10), where isolated populations tuned local conditions are less likely to be success- had evolved from a relatively small gene pool and fully introduced. Even if an introduced parasite per- had no previous experience with many infections sists in a new geographic area, it does not (11). The first epidemics following the arrival of necessarily cause human disease. In the United Europeans were often the most severe. By 1518 or States, humans infected with Taenia solium, the 1519, smallpox appeared in Santo Domingo, where parasite that causes cysticercosis, infrequently it killed one-third to half of the local population and transmit the infection because sanitary disposal of spread to other areas of the Caribbean and the feces, the source of the eggs, is generally available. Americas (10). The population of central Mexico is In short, the likelihood of transmission involves estimated to have dropped by one-third in the single many biological, social, and environmental vari- decade following contact with the Europeans. ables. Travel across the Atlantic Ocean transformed the flora and fauna of the New World as well. Some of the transported materials became important Historical Perspective sources of food (plants), clothing, and transportation Human migration has been the main source of (animals). Other transfers were less welcome: Japa- epidemics throughout recorded history. William nese beetles, Dutch elm disease, and chestnut tree McNeill (7), in his book Plagues and Peoples, de- fungus. A.W. Crosby, exploring these exchanges be- scribes the central role of infectious disease in the tween the Old and the New Worlds, sounds a pessi- history of the world. Patterns of disease circulation mistic note: “The Columbian exchange has left us have influenced the outcome of wars and have with not a richer but a more impoverished genetic shaped the location, nature, and development of pool” (10). human societies. The explorers also paid a price in loss of lives from Trade caravans, religious pilgrimages, and mili- disease. Philip Curtin (12) provides a quantitative tary maneuvers facilitated the spread of many dis- study of “relocation costs,” the excess illness and eases, including plague and smallpox. A map in death among European soldiers in the nineteenth Donald Hopkins’ book, Princes and Peasants: Small- century when they lived or worked in the tropics. pox in History (8), traces the presumed spread of Until the most recent armed conflicts, infectious smallpox from Egypt or India, where it was first diseases claimed more lives than injuries during thought to have become adapted to humans some- wars. time before 1000 B.C. Smallpox spread easily from Plague holds a prominent place in history and person to person through close contact with respira- remains with us today. A bacterial infection caused tory discharges and, less commonly, through contact by Yersinia pestis, it is primarily an infection of with skin lesions, linens, clothing, and other mate- rodents, spread by their fleas. Human infection is rial in direct contact with the patient. Because pa- incidental to the maintenance of Y. pestis in animal 40 Emerging Infectious Diseases Vol. 1, No. 2 — April-June 1995 Perspective reservoirs. Yet plague periodically has erupted in Another type of travel relevant to disease emer- human populations, wreaking great devastation, gence is the shift of populations to urban areas. It is killing millions and causing infection that can be estimated that by the year 2010, 50% of the world’s spread directly from person to person by the respi- population will be living in urban areas. It is pro- ratory route. Human population movement has been jected that by the year 2000, the world will comprise essential in the spread of plague and the dispersal 24 “megacities”—sprawling metropolitan areas with of rodents and their fleas to new areas. For centuries populations exceeding 10 million (World Bank, plague spread along trade routes. It reached Califor- UNDP, World Health Organization, unpublished nia by boat around the turn of this century, caused data). These areas will have the population density epidemic infection in San Francisco, and then to support persistence of some infections and con- spread to wildlife, where it persists today in a large tribute to the emergence of others. Many of these enzootic focus. areas are located in tropical or subtropical regions, where the environment can support a diverse array of pathogens and vectors. Also developing are huge Movement of People periurban slums, populated with persons from many Travel for business and pleasure constitutes a geographic origins. Poor sanitation allows breeding small fraction of total human movement (5,13). Peo- of arthropod vectors, rodents, and other disease-car- ple migrating individually or in groups, may be rying animals. Crowded conditions favor the spread immigrants, refugees, missionaries, merchant ma- of diseases that pass from person to person, includ- rines, students, temporary workers, pilgrims, or ing sexually transmitted infections. Travel between Peace Corps workers. Travel may involve short dis- periurban slum areas and rural areas is common, tances or the crossing of international borders. Its paving the route for the transfer of microbes and volume, however, is huge. In the early 1990s more disease. Transfer of resistance genes and genetic than 500 million persons annually crossed interna- recombination may also occur in and spread from tional borders on commercial airplane flights (World crowded environments of transients. Tourism Organization, Madrid, unpublished data). Acute disturbances, whether climatic or political, An estimated 70 million persons, mostly from devel- lead to interim living arrangements, such as refugee oping countries, work either legally or illegally in camps and temporary shelters, that provide ideal other countries (14). Movement may be temporary conditions for the emergence and spread of infec- or seasonal, as with nomadic populations and mi- tions. Temporary living quarters often share simi- grant workers who follow the crops. Military maneu- larities with periurban slums: crowding, inadequate vers worldwide employ and move huge populations. sanitation, limited access to medical care, lack of The consequences of armed conflict and political clean water and food, dislocation, multiethnic com- unrest displace millions. In the early 1990s, there position, and inadequate barriers from vectors and were an estimated 20 million refugees and 30 million animals. An example is the movement of 500,000- displaced persons worldwide (International Organi- 800,000 Rwandan refugees into Zaire in 1994. Al- zation for Migration, personal communication). most 50,000 refugees died during the first month as Grubler and Nakicenovic estimated and plotted epidemics of cholera and Shigella dysenteriae type 1 the average kilometers traveled daily for the French swept through the refugee camps (17). population over a 200-year period (1800-2000) and Movement into a rural environment poses differ- found that spatial mobility has increased more than ent risks and often places new rural populations in 1000-fold (15). In the last 40 years, the size of Aus- contact with pathogens that are in the soil and water tralia’s population has doubled and the number of or are carried by animals or arthropods (18). Some persons moving into and out of Australia has in- of these pathogens such as Guanarito (19) and Sabià creased nearly 100-fold (16). viruses (20) in South America, were only recently Although social, economic, and political factors recognized as capable of infecting humans. push people from an area or draw them to another, environmental resources and their impact on food and water supplies are behind many conflicts lead- Consequences of Movement ing to displacement of populations. Acute disasters, Human migration favors the emergence of infec- such as flooding, earthquakes, and hurricanes often tious diseases through many mechanisms. When force populations to seek shelter and sustenance in people migrate, they carry their genetic makeup, new lands. Chronic changes, such as drought, deple- their accumulated immunologic experience, and tion of soil, and disappearance of fish from streams, much more (Table 2). They may carry pathogens in lakes, and oceans, draw people to new territories, or, or on their bodies and may also transport disease more frequently, to the fringes of large urban cen- vectors, such as lice. Their technology (agricultural ters. and industrial), methods for treating disease, cul- tural traditions, and behavioral patterns may influ- 41 Vol. 1, No. 2 — April-June 1995 Emerging Infectious Diseases Perspective ence their risk for infection in a new environment permissiveness can pertain to human behavior, the and their capacity to introduce disease into the new environment, or the presence of appropriate vectors region. Their social standing and resources may or intermediate hosts. For example, the ease with affect their exposure to local infections and their which HIV spreads in a population depends on sex- access to adequate nutrition and treatment. People ual practices, condom use, the number of sex part- also change the environment in many ways when ners, and intravenous drug use, among other they travel or migrate—they plant, clear land, build, factors. Malaria requires specific mosquito vectors and consume. Travel is relevant in the emergence of (with access to susceptible humans) to spread to new disease if it changes an ecosystem. The following geographic regions. Schistosomiasis can be intro- examples show the many ways in which migration duced into a new region only if the appropriate snail can influence the emergence of disease in a new area. host is present and if the eggs excreted (in urine or 1. Humans may carry a pathogen in a form that feces, from an infected person), reach the snails in can be transmitted, then or later, directly or indi- an appropriate environment. rectly to another person. The pathogen may be silent 5. Humans may carry a strain of microbe that (during the incubation period, chronic carriage, or has an unusual resistance pattern or virulence latent infection) or clinically evident. Examples in- genes. A multiple-drug-resistant strain of Klebsiella clude hepatitis B virus, human immunodeficiency pneumoniae appears to have been transferred by an virus (HIV), Mycobacterium tuberculosis, M. leprae, asymptomatic woman from a hospital in Bahrain to Salmonella typhi, and other salmonella. Disease Oxford, where it caused outbreaks in two British may be especially severe when a pathogen is intro- hospitals (23). People also carry their background duced into a population that has no previous expo- flora, in the intestinal tract, for example, which may sure to the infection. How long the consequences of contain plasmids and resistance genes that can in- migration persist varies with the specific infection. teract with microbes in a new area. It is not just the The two most critical characteristics are the dura- classic pathogens that may be relevant to the emer- tion of survival of the pathogen in a potentially gence of a new disease but the individual traveler’s infective form and its means of transmission. total microbiologic “baggage.” 2. Epidemic cholera in Africa spread along the 6. Visitors to a region may lack immunity to West African coast and, when the disease moved locally endemic infections, such as hepatitis A and inland, followed fishing and trading routes. Mar- sand-fly fever. Visitors may suffer severe or different kets, funerals, refugee camps—events that involved manifestations of infection or disease at an age when migration of persons and large gatherings with close the local population is immune to it. Resettlement contact—helped spread the infection. With El Tor of populations into malaria-endemic regions can cholera, asymptomatic and mild infections can out- lead to a high death rate from falciparum malaria. number severe disease by 100 to 1 (21), thus permit- 7. Kala-azar caused a deadly outbreak in remote ting those infected to continue to move and work. villages in southern Sudan in 1994. The origin was 3. Pilgrims carried an epidemic strain of group A thought to be the villagers’ exposure to the sand-fly Neisseria meningitidis from southern Asia to Mecca vector during migration to a food distribution center in 1987. Other pilgrims who became colonized with that had been established by a relief organization the epidemic strain introduced it into sub-Saharan (24). The migration took a malnourished population Africa, where it caused a wave of epidemics in 1988 from a nonendemic zone into the southern part of and 1989 (22). the kala-azar–endemic zone. Unfamiliarity with the 4. Humans may carry a pathogen that can be disease and the poor nutritional status of the popu- transmitted only if conditions are permissive. This lation probably contributed to a high death rate (24). 8. Behavioral patterns in a new region may place visitors at risk for infection, while the local popula- Table 2. What is carried by humans into new tion, possibly because of their knowledge of disease regions? risks, may not be at risk. Behavior patterns may Pathogens in or on body involve food preparation (such as eating some foods Microbiologic flora raw), clothing (or lack of it), (for example, going barefooted), sleeping arrangements (sleeping on the Vectors on body ground or out of doors in an unscreened area), and Immunologic sequelae of past infections contact with animals. Vulnerability to infections 9. Susceptibility of a population may vary be- cause of genetic differences. A microbe introduced Genetic makeup into a new region may have a greater or lesser Cultural preferences, customs, behavioral impact, depending on the host population. Genetic patterns, technology factors influence susceptibility to and expression of Luggage and whatever it contains several infectious diseases. Although these interac- 42 Emerging Infectious Diseases Vol. 1, No. 2 — April-June 1995 Perspective tions are not yet well defined for most infections, gens and vectors. The globalization of markets genetic factors influence infections caused by differ- brings fresh fruits and vegetables to dinner tables ent classes of organisms, including cholera (25,26), thousands of miles from where they were grown, parvovirus infection (27), malaria, and Helicobacter fertilized, and picked. Tunnels, bridges, and ferries pylori infection (28). form means to traverse natural barriers to species spread. The roads built to transport people often To determine the consequences of travel both the speed the movement of diseases from one area to traveler and the population visited must be consid- another. Mass processing and wide distribution net- ered. Migration may be in only one direction, though works allow for the amplification and wide dissemi- travel often involves returning to the point of origin, nation of potential human microbes. perhaps after the traveler has made many stops Examples of introduced species include plants along the way. The changes in the various ecosys- and animals—insects, microbes, and marine organ- tems as a consequence of the migration guide the isms. emergence of diseases; any study that simply focuses on the traveler is too narrow. 1. Ships convey marine organisms on their hulls and in their ballast water. For example, 367 differ- The distance traversed is less important than the ent species were identified in ballast water of ships differences in biological life in different areas and traveling between Japan and Coos Bay, Oregon (32). differences in receptivity and vulnerability. In think- Introductions have had devastating effects in some ing about disease emergence, what matters is the areas, for example such as the Black and Azov seas, potential of a disease to appear in a place, popula- where newly introduced jellyfishlike creatures tion, or extent not previously reported. called ctenophores have ruined local fishing (33). What is the long-term impact of migration and 2. Vibrio cholerae may have been introduced to travel on human disease? Carriage of pathogens is South America by shipping (34). Researchers iso- only part of the influence on disease emergence. lated the organism in samples of ballast, bilge, and Introduced technology, farming methods, treatment sewage from 3 of 14 cargo ships docked at Gulf of and drugs, chemicals, and pesticides may have a far Mexico ports. The ships had last ports of call in greater and longer impact on disease patterns in a Brazil, Colombia, and Chile (35). V. cholerae O1, region than the life of a person. Deforestation, build- serotype Inaba, biotype El Tor, indistinguishable ing of dams, and opening of roads into previously from the Latin American epidemic strain, was found inaccessible areas have all been associated with in oysters and oyster-eating fish from closed oyster population movements and changes in distribution beds in Mobile Bay, Alabama (36). V. cholerae O139 and frequency of a variety of infections in humans has spread along waterways in Asia, although the (such as malaria, schistosomiasis, Rift Valley fever, people carried on the boats doubtless played a role and sexually transmitted diseases). (37,38). Increasingly the vehicle of transportation is the 3. Aedes albopictus was introduced into the site or even the source of outbreaks. During travel, United States inside used tires shipped from Asia people from diverse origins are enclosed in close (39,40). The mosquito’s introduction causes concern proximity for a hours or days and then discharged to because it is an aggressive biter, survives in both move on to many distant places. These temporary forest and suburban habitats, and appears to be a new habitats, jumbo jets or huge ocean liners, can competent vector for several human pathogens. It be the sites for dissemination of the microbes (as has been associated with epidemic dengue fever happens, for example with Legionella pneumophila transmission in Asia and is a competent laboratory infections (29), foodborne infections, and cholera) or vector of La Crosse, yellow fever, and other viruses provide a milieu for person-to-person transmission (41). In Florida, 14 strains of eastern equine en- (influenza, tuberculosis (30,31)). cephalitis virus have been isolated from A. albopic- tus (42). The mosquito is now established in at least Shipping and Commerce 21 of the contiguous states in United States and in The biomass of humans constitutes only a frac- Hawaii. tion of the matter moved about the earth. Humans 4. The African anopheles mosquitoes arrived in carry and send a huge volume of plants, animals and Brazil in about 1929. This vector could breed under other materials all over the face of the globe. Much conditions other New World mosquitoes could not. of this movement results from the planned transport Although the malaria parasite was already found in of goods from one place to another, but some is an Brazil, this new vector expanded the range of trans- unintended consequence of shipping and travel. All mission. An estimated 20,000 persons died of ma- has an impact on the juxtaposition of various species laria before the introduced anopheles mosquitoes in different ecosystems. “Hitchhikers” include all were eliminated. manner of biologic life, both microscopic and macro- 5. It has been repeatedly demonstrated that mos- scopic. Animals can carry potential human patho- quitoes are present—and survive—on international 43 Vol. 1, No. 2 — April-June 1995 Emerging Infectious Diseases Perspective flights. In random searches of airplanes in London, As noted already, factors that can influence recep- mosquitoes were found on 12 of 67 airplanes from tivity include climate and environmental conditions, tropical countries (43). Arthropods can survive even sanitation, socioeconomic conditions (50), behavior, more extreme environments. In one study, mosqui- nutrition, and genetics. V. cholerae persists in an toes, house flies, and beetles placed in wheel bays of aquatic reservoir off the Gulf Coast of the United Boeing 747B aircraft survived flights of 6-9 hours States, yet epidemic cholera has not been a problem with external temperatures of -42° C (43). Airplanes in the United States. Where poverty and poor sani- have also carried infective mosquitoes that caused tation prevail, the presence of V. cholerae can be a human infection outside malaria-endemic areas (in source of endemic disease and periodic epidemics. Europe, for example). Disease emergence is often complex. An outbreak 6. Vehicles can transport vectors over land. of malaria in San Diego, California, occurred when Glossina palpalis, a vector for African trypanosomi- parasitemic migrant workers were employed in an asis (sleeping sickness), can fly up to 21 km but can area where mosquitoes capable of transmitting ma- be transported much longer distances on animals laria had access to the workers and to a susceptible and in land vehicles. human population (51). Many conditions had to be 7. Seven persons in Marburg, Germany, died met to allow transmission. after handling blood and tissues from African green Migration may introduce parasites into an area monkeys from Uganda. The tissues contained an where a different intermediate host or vector could organism later named Marburg virus (44). change the incidence of disease. Cycling through a 8. Exotic animals transported from their usual different host can lead to different transmission habitats are clustered in zoos; others are used in rates, different infectivity, and even different clinical research laboratories where they have occasionally expression. A parasite may be more successful in a caused severe disease in humans. Two examples are new site because of a larger susceptible population B virus from primates (45) and hemorrhagic fever or the absence of predators. with renal syndrome from rodents (46). 9. The world trade and globalization of organs, Confluence of Events tissues, blood, and blood products is growing. Re- Massive global travel is taking place simultane- searchers are considering animals as sources for ously with many other processes that favor the tissues and organs for transplantation (47). emergence of disease. For example, the human 10. Plants may not directly cause human dis- population is more vulnerable because of aging, im- ease. But they can alter an ecosystem and facilitate munosuppression from medical treatment and dis- the breeding of a vector for human disease. This can ease (such as AIDS), the presence of prostheses (e.g., also displace traditional crops that provide essential artificial heart valves and joints), exposure to chemi- nutrition. Vertical transmission of plant pathogens cals and environmental pollutants that may act (and spread of plant diseases) can result from seed synergistically with microbes to increase the risk of movement (48). Carriage of seeds into new areas can diseases, increased poverty, crowding and stress, introduce plant pathogens. and increased exposure to UV radiation. Technologic 11. Migration and altered environments have in- changes, while providing many benefits, can also creased the so-called weedy species. These species promote disease dissemination. Resistance of mi- migrate easily and have high rates of reproduction. crobes and insects to antimicrobial drugs and pesti- If they lack local predators, they can displace other cides interferes with the control of infections and species and often upset local ecology. allows transmission to continue. Changes in land use can alter the presence and abundance of vectors Introduction of Species into New Areas and intermediate hosts. Microbes are enormously resilient and adaptable. Introducing species into new geographic areas is They have short life spans, which allow rapid genetic not new, but the current volume and frequency of change. Humans, by comparison, are slow to change introductions are unprecedented. A pathogen’s sur- genetically but can change their behavior. People vival and spread in a new environment are deter- move and construct barriers to prevent contact with mined by its basic reproductive rate, which is the microparasites, macroparasites, and the extremes of average number of successful offspring a parasite the environment. Technology fosters a perception of can produce (49). To invade and establish itself in a human invincibility but actually creates new vulner- host population, a parasitic species must have a abilities, as it enables us to go deeper, higher, and basic reproductive rate exceeding one (49). The sim- into more remote and hostile environments. Studies plicity of this statement belies the complexity of show that no place on earth is devoid of microbes. circumstances that influence invasion and persist- Their range and resiliency are truly phenomenal. ence. These circumstances encompass biological, so- Only a fraction of the existing microbes have been cial, and environmental factors. 44 Emerging Infectious Diseases Vol. 1, No. 2 — April-June 1995

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