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30 The ViralSuperhighway CeorgeArmelagos Anthropologists look at human health through the wide-angled lens of our species'slong evolutionary history, our biology in a world of microorganisms,and the remarkable medical achievementsof our culture. Anthropologists try to seethe "big picture." epidemiologists-scientists As recentlyasthe 1970s, who study the spread of disease-were publicly saying that the ageof infectiousdiseasewas a thing of the past. At that time, it appearedthat the world's major killers, including polio, smallpox, and tuberculosis, were urder control-or at leastthat biomedical science had developed the methods to get them under control. But that has not been the case.Recent decadeshave seen the emergence of a growing list of new infectious diseases(like HIV/AIDS and SARS) as well as the resurgence of old diseases (like tuberculosis and malaria). This selection,written by a leading biological anthropologist,showshow pathogenicmicroorganisms evolve along with humans (and other species)in conjunction with major shifts in patterns of human residence, technological development, and travel. The author identifies three major shifts in the overall pattern of human disease, or "epidemiological transitions," and links them with three major episodes in human prehistory and history. The first shift involved the domesti.cationof plants and animals that made humans change from nomadic hunting and gathering to sedentary agricultural patterns of residence. The second epidemiological trarsition was associatedwith the improvements in nutrition, hygiene, and medicine that accompanied the lndustrial Revolution in the nineteenth century and has been characterized by the decline of infectious diseaseand an increasein chronic diseasein the developedworld. This second transition has primarily happened in rich countries. The third epidemiological trarrsition, taking place as we speak,is the result of contemporaiy patterns of globalizatiory ranging from global warming and other forms of environmental degradation to new patterns of slobal havel and corr[nerce. Another major contributor to this third shift is the emergenceof drug-resistant strains of common diseases.As the selectionillustrates, the pathogens that cause infectious disease,like all other living organisms, are constantly evolving and adapting to new environments. This new development-drug-resistant strainsof common microbes-is one of the most frightening possibilities humans now face. However, contemporary human societiescan take concretestepsto counter the threats posed by the "viral superhighway." Taking those steps, however, will require concertedeffort by political leaders,public health experts, and by all of us. As you read this selection,ask yourself the follozning questions: Armelagos, George. "The Viral Superhighway." This article is repdnted by permission of the New York Academy of Sciences from THE SCIENCES[an/Feb 1998):24-29. 202 r r How is population health influencedby culture? l^hat is an "epidemiologicaltransition?" r The author describesnot one but three epidemioIosical transitionsover the courseof human history. \,\trhendid each of these transitions occur in Europe and the United States,and how can each be explained? r How is globalization involved in the increasingly rapid spreadof infectiousdisease? r l^tlat steps can we take to protect ourselves, and future generations,againstthe dangersposedby the widening "viral superhighway" ? Thefollozoing terms discussedin this selectionare included in the Glossary at the back of thebook: diseasesofcinilization gicaI tr ansit ion epi demiolo pathogen THEVIRALSUPERHICHWAY uponIsraelftom themoming SotheLod senta pestilence until theappointedtime;andtherediedof thepeople ftom thousandmen Dan to Beershebasetsentu -2 Sam.24:15 ing locusts,riversfouledwith )war-s of crop-destro) blood, lion-headedhorsesbreathhg fire and sulfur: the Bible presentsa lurid assortmentof plagues,described as acts of retribution by a vengeful God. lndeed, realllfe epidemics-such as the influenza outbreakof 1918, which killed 21 million peoplein a matter of monthscan be so sudden and deadly that it is easy,even for nonbelievers,to view them asangry messagesfrom the beyond. How reassuring it was, thery when the march of technology began to give people some control over the scourgesof the past. ln the 1950sthe Salk vaccine, and later, the Sabin vaccine, dramatically reduced the incidence of polio. And by 1980 a determined effort by health workers worldwide eradicatedsmallpox,a dise,rsethat had affUctedhumarkind since eail.iesttimes with blindness, disfigurement, and death, killing nearly 300million people in the twentieth century alone. But those optimistic yearsin the secondhalf of our century now seem,with hindsight, io have been an era of inflated expectations,even arrogance.In 1967 the surgeongeneralof the United States,William H. Stewart, announced that victory over infectious diseaseswas imminent-a victory that would close the book on modern plagues.Sadly,we now know differently.Not only have deadly and previously unimagined new illnessessuchasAIDS and Legionnaires'diseaseemerged in recent years,but historical diseasesthat just a few decadesago seemedto have been tamed are returning in virulent, drug-resistarLtvarieties. Tuberculosis,the ancient lung disease that haunted nineteenth-century Europe,afflicting, among others,Chopiry Dostoyevski, and Keats, is aggressivelymutating into strains that defy the standard medicines; as a result, modern TB victims must undergo a daily drug regimen so elaborate that health-departm€ntworkers often have to personally monitor patientsto make sure ihey comply [see "A Plague Retums," by Mark Earnest and John A. Sbarbaro,September/October19931.Meanwhile, bacteria and viruses in foods from chicken to strawbenies to alfalfa sprouts are sickening as many as 80 million Americanseachyear. And those are only symptoms of a much more seneral threat. Deaths from hfectious diseasesin the U.rited States rose 58 percent between 1980 and 1992. Twenty-nine new diseaseshave been reported in the past twenty-five years, a few of them so bloodcurdling and bizarre that descriptions of them bring to mind tacky horror movies. Ebola virus, for instance,can in 203 just a few days reduce a healthy person to a bag of teeming flesh spilling blood and organ parts from every orifice. Creutzfeldt-Jakob disease, which killed the choreographerGeorgeBalanchinein 1983,eatsaway at its victims'brains until they resemblewet sponges. Never slow to fan masshysteria, Holly-wood has capitalized on the phenomenon with films such as Outbreak,ht which a monkey carrying a deadly new virus from central Africa infects unwitting Califomians arLdstarts an epidemic that threatensto annihilate the human race. The reality about infectious disease is less sensational but alarming nonetheless.Gruesome new pathogens such as Ebola are unlikely to cause a widespread epidemic becausethey sicken and kill so quickly that victims canbe easilyidentified and isolated;on the other hand, the seemingly irnocuous practice of overprescribing antibiotics for bad colds could ultimately lead to untold deaths, as familiar germs evolve to become unteatable. We are living in the twilight of the antibiotic era: within our lifetimes, scraped knees and cut fingers may return to the realm of fatal conditions. Through intemational travel, global col nerce, and the acceleratingdestruction of ecosystemsworld, wide, people are inadvertently exposingthemselvesto a Pandora'sbox of emergingmicrobial threats.And recent rumblings about biological terodsm have highlighted the appalling potential of diseaseorganisms for being manipulated to vile ends. But although it may appear that the apocalypsehas arrived, the truth is that people today are not facing a unique predicament. Emerging diseaseshave long loomed like a shadow over the human race. Peopleand pathogenshave a long history together. Infections have been detectedin the bones of human ancestorsmore than a million years old, and evidence from the mummy of the Eg)?tian pharaoh Ramses V suggests that he may have died from smallpox more than 3,000years ago. Widespreadoutbreaksof disease are also well documented. Between 1347 and 1351 roughly a third of the population of medieval Europe was wiped out by bubonic plague,which is carried by fleas that live on rodents. In 1793,10 percent of the population of Philadelphia succumbed to yellow fever, which is spreadby mosquitoes.And in 1875the son of a Fiji chief came down with measles after a ceremonial trip to Australia. Within four months more than 20,000 Fijians were dead from the imported disease, which spreadsthrough the air when its victims cough or sneeze. According to conventional wisdom in biology, people and invading microorganismsevolve together: people gradually become more resistanL and the rnicroorganisms become less virulent. The result is either mutualism, in which the relation benefitsboth species,or commensalism, in which one speciesbenefit:wiihout 204 A ,N D H E A L I N C CULTURE R,E L I C I O N harming the other Chicken pox and measles,once fatal afflictions, now exist in more benign forms. Logic wotrld suggest, after all, that the best interests of an orgarism are not served if it kills its hos! doing so would be like picking a fight with the person who signsyour paycheck. But recentlyit has becomeclearto epidemiologists that the reverseof that cooperativeparadigm of ilJr-ress can alsobe true: microorganismsand their hostssometimes exhaust their energies devising increasingly powerful weaporuy and defenses.For example, several variants of human immuno-deficiencyvirus (HIV) may compete for dominance within a person's body, placing the immune system under ever-greatersiege. As long as a virus has al effective mechanism for jumping from one person to anothet it can afford to kill its victims fsee"The DeadliestVirus," by Cynthia Mills, ]anuary/ February 19971. If the competition were merely a question of size,humanswou ld surelywir: theaveragepersonis l0l7times the size of the average bacterium. But human beings, after all, constitute only one species,which must compete with 5,000kinds of viruses and more than 300,000 speciesofbacteria.Moreovet in the twenty yearsit takes humans to produce a new generation, bacteda car reproduce a half-million times. That disparity enables pathogens to evolve ever more viru lent adaptations that quicldy outstrip human responsesto them. The scenario is govemed by what the English zoologist Richard Dawkins of the University of Oxford a:rd a colleague have called the "Red Queen Principle." In Lewis Carcoll's Throughthe LookingGlzssthe Red Queen tells Alice she will need to r-ul1faster and faster just to stay in the sameplace. Staving off illness can be equally elusive. The Centers for DiseaseControl and Prevention (CDC) in Atlanta, Georgia,has compiled a list of the most recent emerging pathogens. They include: . Campylobacter, a bacterium widely found in chickof the commercialpracticeof raising because ens in cramped, ulhealthy conditions. It causes them million and eight million casesof two between year in the United Statesarrd food poisoning a between200and 800deaths . Escherichia coli 01.57:H7 , a dangerouslymutated version of an often harmlessbacterium. Hamburger meat from jack in the Box fast-food restaurantsthat was contaminatedwith this bug led to the deathsof at leastfour people in 1993. . Hantaviruses, a genus of fast-acting, lethal viruses, often carried by rodents, that kill by causing the capillariesto leakblood.Anew hantavirusknown assin nombre(Sparishfor "nameless")surfacedin 1993in the southwestem United States,causing the sudden and mysterious deaths of thirty-two peoDle. . HIV, the deadly virus that causesAIDS (acquired immunodeficiencysyndrome).Although it was first obserwedin people as recentlyas 1981,it has spreadlike wildfire and is now a global scourge, affectingmore than 30 million people worldwide. . The strangenew infectiousagentthat causes bovine spongiform encephalopathy,or mad cow disease,which recently threw the British meat industry and consumersinto a panic. This bizarre agent,known as a prion, or "proteinaceousinfectious particle," is also responsiblefor CreutzfeldtJakobdisease,the brain-eaterI mentioned earlier. A Nobel Prize was awarded to the biochemist StanleyB. Prusiner of the University of California, SanFrancisco,for his discoveryof the prion. . Legionella pneumophila, thebacter'rwnthat causes Legionnaires'disease.The microorganismthrives in wet environments; when it lodges in airconditioning systemsor the mist machinesin supermarketproduce sections,it can be expelled into the air, reaching people's lungs. In 1976thirtyfour participants at an American Legion convention in Philadelphia died-the incident that 1edto the discovery and naming of the disease. . Bofteliaburgdorferl,the bacterium that causes L)..rnedisease.It is carried by ticks that live on deer and white-footed mice. Left untreated,it can causecrippling, chronhcproblemsin the nerves, joilts and ilternal organs. How ironic, given such a rogues' gallery of nasty characters,that iust a quarter-centuryago the Egyptian demographer Abdel R. Omran could obseruethat ir many modern industrial nations the major killers were no longer infectious diseases.Death, he noted, now camenot from outsidebut rather from withir-rthe body, the result of gradual deterioration. Omral traced the changeto the middle of the nineteenth century,when the industrial revolution took hold in the United States and parts of Europe. Thanks to better nutrition, improved pubJic-healthmeasures,ald medical advances suchasmassimmunization arLdthe introduction of antibiotics, microorganismswere brought under control. As people began living longer, their aging bodies succumbed to "diseasesof civilization:" cancer,clogged arteries, diabetes, obesity, and osteoporosis.Omran was the first to formally recognlzethat shift in the disease environment. He called it an "epidemiological transition." Like other anthropologists of my generatiory I learned of Omran's theory early in my career, and it soonbecameabasic tenet-a comforting one,too, implying asit did alr end to the supremacy of microorganisms. Then, three years ago, I began working with the anthropologist Kathleen C. Bamesof JohnsHopkins University THEVIRALSUPERHICHWAY in Baltimore, Maryland, to formulate an expansion of Omran's ideas.It occurredto us that his epidemiological trarsition had not been a unique event. Throughout history human populations have r.rndergoneshifts in their relations with disease-shifts, we noted, that are always linked to major changesin the way people interact with the environment. Bames and I, along with JamesLin, a master's student at Johns Hopkins University Schoolof Hygiene and Public Health, have sincedeveloped a new theory: that there have been not one but tfuee major epidemiological hansitions; that eachone has been sparked by human activities; and that we are living through the third one right now. The first epidemiological transition took place some 10,000years ago/ when people abandonedtheir nomadic existenceand began farming. That profoundly new way of life disrupted ecosystemsand created denserliving conditionsthat led, asI will soondetait to new diseases. The second epidemiological transition was the salutary one Omran singled out in 1921,when the war againstinfectiousdiseasesseemedto havebeen won. And in the past two decadesthe emergenceof illnessessuch ashepatitisC, cat scratchdisease(caused by the bacterium Bartonellahenselae), Ebola,and others on CDC's list has createda third epidemiologicaltrarsitiory a disheartening set of changesthat in many ways have reversed the effects of the second transition and coincide with the shift to globalism. Burgeoning population growth and urbanization, widespread environmental degradation, including global warming and tropical deforestation,and radically improved methods of transportationhave given rise to new ways of contracting and spreadingdisease. We are, quite literally, making ourselves sick. \,\y'henearly human ancestorsmoved {rom African forests onto the savalna millions of years ago, a few diseasescame along for the ride. Those "heirloom" species-thus deslgnated by the Australian parasitologist J.F.A.Sprent becausethey had afflicted earlier primates-included headandbody lice;parasiticworms such as pinworms, tapeworms, and liver flukes; and possiblyherpesvirus and malaria. For 99.8percentof the five million years of human existence,hulting and gathering was the primary mode of subsistence.Our ancestorslived in small groups arrd relied on wild animals and plants for their survival. In their foraging rounds, early humans would occasionally have contracted new kinds of illrLessesthrough insect bites or by butchering and eating disease-ridden animals.Sucheventswould not haveled to widespread epidemics,however,becausegroups of people were so sparseand widely dispersed. About 10,000years ago, at the end of the last ice age, many groups began to abandon their nomadic lifestyles for a more efficient and secureway of life. The 2O5 agricultural revolution first appeared in the Middle East;later, farming centers developed independently in China and Central America. Permanent villages grew up, and people tuned their attention to crafts such as toolmaking and pottery. Thus when people took to cultivating wheat and barley, they plarLtedthe seedsof civilization as wel1. With the new ways, however, came certain costs. As wild habitats were transformed into urban settings, the farmerswho broughtin the harvestwith their flintbladed sickles were assailedby grim new ailments. Among the most corrlmon was scrub typhus, which is carried by mites that live in tall grasses,and causesa potentially lethal fever Clearing vegetation to create arable fields brought farmers frequently into miteinfested terrain. Irrigation brought further hazards. Standing thighdeep in watery canals,farm workers were prey to the worms thal causeschistosomiasis. After tivine within aquaticsnaiJ:durhg Lheirlarval stage,thoseworms emerge in a free-swimming form that can penetrate human skin, lodge in the intestine or urinary trac! and causebloody urine and other seriousmaladies.Schistosomiasis was well known in ancient Egypt, where outlying fields were irrigated with water frorn the Nile River; descriptions of its symptoms and remedies are presewedin contemporarymedicalpap)auses. The domestication of sheep, goats, and other animals cleared another pathway for microorganisms. With pigs in their yards and chickens roaming the streets, peoplein agriculturalsocieties wereconstartly vulnerable to pathogens that could cross interspecies barriers.Mary suchorganismshad long sincerelched commensalism with their animal hosts, but thev were highly dangerousto humans.Milk from inJectei caftle could transmit tuberculosis, a slow killer that eatsaway at the lu-ngsand causesits victimsto coughblood ani pus. Wool and skinswere loadedwith a*hra'., which can be fatal when inhaled and, in modem times, has been developedby severalnations as a potential agent of biological warfare. Blood from infected cattle, injectedinto peopleby biting insectssuchasthe tsetsefly, spreadsleepingsickness,an often-fataldiseasemarked by tremors and protracted lethargy. A secondmajor effect of agriculture was to spur popuJationgrowth and, perhapsmoreimportant,dinsity.Citieswith populationsashigh as50,000haddeveloped in the Near East by 3000u.c. Scavengerspecies such as rats, mice, and sparrows, which congregate wherever large groups of people live, exposed city dwellers to bubonic plague, typhus, and rabies.And now that people were crowded together,a new pathogen could quickly start an epidemic. Larger populations also enableddiseasessuchasmeasles,mumps, chickenpor; and smallpox to persist in an endemic form-always 206 A ,N D H E A L I N C R ,E L I C I O N CULTURE present, afflicting Part of the population while sparing those with acquired immunitY. Thus the birth of agriculture launched humanity on a trajectory that has again and again brought people into contact with new pathogens. Tilling soil and raising livestock 1edto more energy-intensive ways of extricting resources from the earth-to lumbering, coal mining, oil drilling. New resourcesled to increasingly complex social organization, and to new and more frequent contacts between various societies. Loggers today who venture into the rain forest disturb Previ ously untouched creatures and give them, for the first time, the chance to attack humans But there is nothing new about this drama; only the players have char-rged. Some2,000years ago the introduction of iron tools to sub-SaharanAfrica led to a slash-and-bum style of agriculture that brought people into contact wltl\ Anopheles gambiae,anosqtito that transmits malaria. Improved trarsportation methods also help diseasesextend their reach:microorganismscannottravel far on their own, but they are expert hitchhikers. \Artren the Spanish invaded Mexico in the early 1500s,for instance, they brought with them diseasesthat quickly raged through Tenochtitl6n, the stately, temple-filled capital of the Aztec Empire. Smallpox,measles,and influenza wiped out millions of Central America's original inhabitants, becoming the invisible weapon in the Europeanconquest. L:r the past three decades people and their inventions have drilled, polluted, engineered,paved, planted, and deforested at soaring rates, changing ihe biosphere faster than ever before. The combined effects cary without hyperbole, be called a global revolution. After all, many of them have worldwide repercussions:the widespread chemicalcontaminationof waterways,the thinning of the ozone 1ayer,the loss of speciesdiversity. And such global human actionshave Put Peopleat dsk for infectiousdiseasesin newly complex and devastating ways. Global warming, for instance, could expose mlllions of people for the first time to malaria, sleeping sickness,and other insect-bome illnesses;in the United States, a slight overall temPerature increase would allow the mosquitoes that carry dengue fever to survive as far north as New York CitY. Major changes to the landscape that have become possible in the past quarter-century have also triggered After the constructionof the Aswan Dam new diseases. rn 1970, tor instance, Rift Valley fever idected 200,000 people in Eg1pt, killing 600. The disease had been known to affect livestock, but it was not a maior problem in people until the vast quantities of dammed water becamea breeding grould Ior mosquitoes The insects bit both cattie and humans, helping the virus jump the interspeciesbarrier. kr the eastem United States, suburbanization, another relatively recent phenomenory is a dominant factor in the emergenceof L)..rnedisease-10,000 casesof which are repoded armually. Thanks to modem earthmoving equipment, a soaring economy,and population pressures, many Americans have built homes in formerly remote, wooded areas.Nourished by lawns and gardens and unchecked by wolves, which were exterminated by settlerslong ago, the deer population has exploded, exposing people to the ticks that carry Lyme disease. Meanwhile, widespread pollution has made the oceans a breeding ground for microorganisms. Epidemiologistshave suggestedthat toxic algal bloomsfed by the sewage, fertilizers, and other contaminants that wash into the oceans-harbor countless viruses and bacteria. Thrown together into what amounts to a dirty genetic soup, those pathogens can urtdergo geneswapping and mutations, engendering newly antibioticresistant strains. Nautical tra{fic can carry ocean pathogens far and wide: a devastating outbreak of cholera hit Latin America in 1991after a ship from Asia udoaded its contaminated ballast water into the harbor of Callao, Peru. Cholera causesdiarrhea so severeits victims can die in a few days from dehydration; in that outbreak more than 300,000 people became ill, and more than 3,000died. The modem world is becoming-to paraPhrase words of the microbiblogist Stephen S. Morse of the Columbia University-a viral superhighway. Everyone is at risk. Our newly global society is characterized by huge increasesin populatiory intemational travef and international trade-factors that enable diseasesto spread much more readily than ever before ftom Person to person and from continent to continent. By 2020the world population will have surpassed seven billion, and half those people will be living in urban centers. Beleaguered third-wor1d nations are already hard-pressed to provide sewers, plurnbing, and other inJaastructure;in the future, clean water and adequate sarritation could become increasingly rare. Meanwhile, political upheavals regularly cause millions of people to flee their homelands and gather in refugee camps,which become petri dishes for germs. More than 500 million people cross intemational borders eachyear on commercial flights. Not only does that traffic volume dramatically increase the chance a sick person will infect the inhabitants of a distant area when she reaches her destination; it also exposes the sick person'sfellow passengersto the disease,because of poor air cilculation on planes. Many of those Passengers can, in tum, pass the disease on to others when thev disembark. THEVIRALSUPERHICHWAY The global economy that has arisen in the past two decades has established a myriad of cornections between far-flung places. Not too long ago bananas and oranges were rare treats in northem climes, Now you can walk into your neighborhood market and find food that has been flown and trucked in from all over the world: oranges from Israel, apples from New Zealand, avocados from California. Consumers in affluent nations expect to be able to buy whatever they want whenever they want it. l trhat people do not generally realize, however, is that this global network of food production and delivery provides countless pathways for pathogens. Raspberries from Guatemala, carrots from Peru, and coconut milk from Thailand have been responsible for recent outbreaks of food poisoning in the United States. And the problem cuts both ways: contaminated radish seeds and frozen beef from the United Stateshave ended up in Japan and South Korea. Finally, the widespread and often indiscrirninate use of antibiotics has played a key role in spuning disease. Forty million pounds of antibiotics are manufactured annually in the United States,an eightyfold increasesince 1954.Dangerous miooorganisms have evolved accordingly, often developing antibiotic-resistantstrains.Physicians are now faced with penicillin-resistant gonorrhea, multiple-drug-resistant tuberculosis, and E. coll variants such as 0157:H7.And frighteningly, some enterococcus bacteria have become resistarrt to nll known antibiotics. Enterococcusinfectionsarerare,but staphylococcusin{ections are not, and rr.any strains of staph bacteria now respond to just oneantibiotic, vancomycin.How long will it be before run-of-the-mill staph infections-in a boil, for instance,or in a surgical incision-become r,rntreatable? Although civilization can expose people to new pathogens,cultural progressalsohas an obvious countewailing effechit canprovide tools-medicines, sensible 207 city planning, educational campaigns about sexually transmitted diseases-to fight the encroachments of disease.Moreover,sincebiology seemsto side with microorganisms any'way, people have little choice but to depend on protective cultura1 practices to keep pace: vaccinations, for instance, to confer immunity, combined with practices such as hand-washing by physicians between patient visits, to limit contact between peopleand pathogens. A11too oftery thougtu obvious protective measures such as using only cleanhypodermic needlesor treating urban drinking water with chlorine are neglected, whether out of ignorance or a wrongheaded emphasison the short-term financial costs.Theworldwide disoaritv in weallh is also to blame:not suprisingly, the advances made during the secondepidemiological transition were limited largely to the affluent of the industrial world. Such lapses are now begirming to teach the bitter lesson that the delicate balance between humans and invasive microorganisms carr tip the other way again. Overconfidence*the legacy of the second epidemiological tralsition-has made us especially vulnerable to emerging ald reemerging diseases. Evolutionary principles can provide this useful corrective: in spite of al1 our medical and technological hubris, there is no quick fix. If human beings are to overcome the current crisis, it will be through sensible changes in behavior, such as increased condom use and improved sanitation, combined with a coiunitment to stop disturbing the ecological balance of the planet. The Bible, in short was not far {rom wrong: We do bring plagues upon ourselves-not by sinning, but by refusing to heed our own alarms, our own best judgment. The price of peace-or at least peaceful coexistence-with the microorganisms on this planet is eternalviqilance.