The Viral Storm

by Nathan Wolfe

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  The use of boats to visit new lands would continue with increasing frequency over the forty or so thousand years following this first colonization of Australasia. We have much better knowledge of what later trips were like and how they connected microbially distant lands. Perhaps the peak of boating-based colonization before modern times occurred among the Polynesian populations of the South Pacific.

  Among these Polynesian journeys, probably the most incredible was the first discovery of Hawaii, over two thousand years ago.2 For the first lucky settlers, finding this island would have been truly like finding a needle in a haystack. To give a sense of scale, the largest island of the Hawaiian archipelago, also named Hawaii, has a diameter of around a hundred miles. And the Southern Marquesas, whose inhabitants were the most likely first colonizers of Hawaii, are some five thousand miles away. To imagine what it would have been like to hit the mark, imagine we blindfolded an Olympic archer, then spun him around and asked him to hit his target—the ratios are about the same. One can only imagine how many boats (and their inhabitants) were lost before the fortunate finally made it.

  On their long trips, the Polynesians probably lived largely on caught fish and rainwater. Yet they traveled with a veritable biological menagerie. They brought along sweet potatoes, breadfruit, bananas, sugarcane, and yams. They also traveled with pigs, dogs, chickens, and probably (unintentionally) rats. Having all of these domesticated species meant that the flotillas carried not only life support for the Polynesian explorers, but also minirepositories of microbes, which would spread and mix with local microbes in the places that they discovered.

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  The boat journeys of the Polynesians, as remarkable as they were for their time, pale in comparison to the global shipping that emerged in the fifteenth and sixteenth centuries. By the time Europeans reached the New World, in the late fifteenth century, thousands of massive sailing ships were plying the waters of the Atlantic and Indian Oceans and the Mediterranean Sea, moving people, animals, and goods back and forth between the countries of the Old World.

  The impact of smallpox on New World populations is the most dramatic known example of the way that the connections formed by shipping can influence the spread of microbes. Some estimates suggest that as many as 90 percent of the people living in the Aztec, Maya, and Inca civilizations were killed by smallpox brought by boats during European colonization, a massive and devastating carnage. And smallpox was only one of many microbes that spread along the shipping routes of this time.

  Each of the major transportation advances would alter connectivity between populations, and each would have their own impact on the spread of new microbes. The exclusivity of ships as a means for long-distance transport would not hold out forever. The use of roads, rail, and air provided new connections and routes for the movement of humans and animals as well as their microbes. For microbes, the transportation revolution was really a connectivity revolution. These technologies created links that forever changed the nature of human infectious diseases, including, critically, how efficiently they spread.

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  The use of roads of some sort or another is an ancient practice, far predating the use of water as a medium for transportation. Chimpanzees and bonobos both create and use forest trails to help them move through their territories. I learned this firsthand while studying wild chimpanzees in the Kibale Forest National Park in southwest Uganda. Richard Wrangham, the Harvard professor who introduced me to this work, used these trails to help observe chimpanzees.

  Wrangham had done his doctoral work at the Gombe Stream site in Tanzania that Jane Goodall established. He’d critiqued some of the findings from Gombe because the chimpanzees there were habituated by provisioning—to get the wild chimpanzees comfortable with human researchers, the animals were fed large amounts of banana and sugarcane. Wrangham felt that provisioning changed some of the subtle chimpanzee behaviors, so when he started his own site in Kibale, he habituated the animals the hard way—by having his teams follow them until the apes effectively gave up and no longer ran away. He did this by essentially enhancing and extending the natural pathways that they moved along.3

  The art of actual road building began in earnest around five to six thousand years ago when cultures throughout the Old World started using stone, logs, and later brick to enable the movement of people, animals, and cargo. The first modern roads followed in the late eighteenth and nineteenth centuries in France and the United Kingdom. These roads used multiple layers, drainage, and eventually cement to make permanent structures permitting regular movement throughout the year.

  The rate at which modern roads have spread throughout the world has not been consistent, of course. Some regions in Europe and North America have roads reaching most human populations, while some regions where I work in central Africa have virtually no road access. Clearly, as roads enter into new regions, they bring both positive and negative effects. They are among the top priorities for many rural communities since they provide access to markets and health care, but from the perspective of global disease control, they are double-edged swords.

  HIV is among the most notable example of the impact that road proliferation has had on the movement of microbes. In a series of fascinating studies, the HIV geneticist Francine McCutchan, whose lab I worked in at Walter Reed Army Institute of Research (WRAIR), and her colleagues at the Rakai and Mbeya sites in east Africa have examined the role that roads have played in the spread of HIV, demonstrating that proximity to roads increases a person’s risk of acquiring HIV. As people have more access to roads, they have a higher chance of getting infected because roads spread people, and people spread HIV. Other than sex workers, the highest occupational risk for acquiring HIV in sub-Saharan Africa is being a truck driver. McCutchan and her colleagues have shown that the genetic complexity of HIV is greater among individuals who have increased access to roads. Roads provide the mechanism for different types of HIV to encounter one another, in a single coinfected individual, and swap genetic information. But roads do more than just help established viruses spread. Roads and other forms of transport can also help to ignite pandemics.

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  One of the most stubbornly lingering public misconceptions is that we don’t know how HIV originated. In fact, our understanding of the origins of HIV is more advanced than our understanding of the origins of probably any other major human virus. As we saw in chapter 2, the pandemic form of HIV is a chimpanzee virus that crossed into humans.4 There is no debate within the scientific community on this point. The cumulative evidence with regard to how it originally entered into humans is also increasingly unequivocal. It was almost certainly through contact with chimpanzee blood during the hunting and butchering of chimpanzees. We’ll delve further into this in chapter 9 when we discuss the work my colleagues and I have done with central African hunters.

  Perhaps the only lingering debate about HIV origins is how it originally spread from the first infected hunter and why it took so long for the medical community to discover it. The earliest historical HIV samples date from 1959 and 1960, twenty years before AIDS was even recognized as a disease. In an amazing piece of viral detective work, evolutionary virologist Michael Worobey and his colleagues managed to analyze a virus from a specimen of lymph node from a woman in Leopoldville, Congo (now Kinshasa, DRC).

  The lymph node had been embedded in wax for over forty-five years. By comparing the genetic sequence of the virus they found in the specimen with other strains from humans and chimpanzees, they were able to attach rough dates for the first ancestor of the human virus. While the genetic techniques they used cannot pinpoint dates closer than a few decades, they concluded that the virus split from the lineage sometime around 1900 and certainly before 1930. They also concluded that by the time that the woman in Leopoldville became infected with HIV in 1959 there was already a significant amount of genetic diversity of HIV in Kinshasa, suggesting that the epidemic had already established itself there
.

  The fact that HIV goes back to 1959, let alone 1900, provides some serious challenges to the medical community. One of the central questions is this: if it was in human populations in the early twentieth century and already constituted at least a localized epidemic in Kinshasa by 1959, why did it take us until 1980 to identify the epidemic? Another key question is what special conditions were present that permitted the virus to start taking off in the middle of the twentieth century?

  A number of changes occurred in francophone central Africa, the region where HIV-1 originated, leading up to the period in the 1950s when those first precious samples were taken. The anthropologist Jim Moore and his colleagues at the University of California, San Diego, put together some of the key events in a 2000 paper, the majority of which focused on how easier means of travel influenced virus proliferation. In 1892 steamship service began from Kinshasa to Kisangani in the very heart of the central African forest. The steamship service connected populations that had been largely separated, creating the potential for viruses that previously might have gone extinct in local isolated populations to reach the growing urban centers. In addition, the French initiated the construction of railroads, which, like shipping and road lines, connect populations. This produced another mechanism for viruses to spread from remote regions to urban centers, effectively providing a larger population size of hosts for a spreading virus.

  In addition to the connectivity provided by new steam, rail, and road lines, the construction of railroads and other large infrastructure projects led to cultural changes that also had an important impact. Large groups of men were conscripted, often forcefully, to build railroads. Moore and his colleagues note that the labor camps were populated mostly by men, a condition that dramatically favors transmission of sexually transmitted viruses like HIV. Together, the shipping and rail routes and the factors surrounding their construction must have played a role in the early transmission and spread of HIV.

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  As dramatic as the road, rail, and shipping revolutions were for the transmission of microbes, an entirely new form of transport would add another layer of speed. On December 17, 1903, in Kitty Hawk, North Carolina, a site chosen for its regular breeze and soft sandy landing areas, the Wright Brothers made the first sustained, controlled, and powered flight. Some fifty years later the first commercial jet flew between London and Johannesburg. By the 1960s, the age of jet travel was here to stay.

  Airplanes link populations in an immediate way, which allows the transmission of microbes to occur even more quickly. Microbes differ from each other in terms of their latent period, the period of time between when an individual is exposed and when they become infectious or capable of transmitting the agent to others.5 Almost no microbes that we know of have latent periods of less than a day or so, but many have latent periods of a week or more. The immediacy of air travel means that even microbes with very short latent periods can spread effectively. In contrast, if a person infected with an agent that had a very short latent period were to board a ship, unless the ship had hundreds of individuals the virus could infect, it would go extinct before the ship made land.

  Top: World air traffic, 1933; Bottom: World air traffic, 2010. (T: Dusty Deyo; B: OpenFlights.org)

  Commercial air flights alter in fundamental ways how epidemic disease spreads. In a fascinating paper from 2006, my colleagues John Brownstein and Clark Freifeld of Harvard, one of the new academic breed of digital epidemiologists, found creative ways to use existing data to show just how much impact air travel has on the spread of influenza. John and his colleagues analyzed seasonal influenza data from 1996 to 2005 and compared it with patterns of air travel. They found that the volume of domestic air travel predicts the rate of spread of influenza in the United States. Interestingly, the November travel peak around Thanksgiving appears to be of particular importance. International travel also plays a vital role. When the number of international travelers is lower, the peak of the influenza season comes later—because when there are fewer travelers, it takes longer for the virus to spread. Perhaps most strikingly the researchers were able to see the impact of the terrorist attacks of September 2001 on influenza. The travel ban led to a delayed influenza season. The striking effect was not seen in France, which did not enact the ban, providing an excellent control.

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  During the past few centuries the ease of movement has increased dramatically throughout the world. The rail, road, sea, and air revolutions have all permitted humans and animals to move more quickly and efficiently both within continents as well as between them. The transportation revolution has created interconnectivity unprecedented in the history of life on our planet. It is estimated that we now have over fifty thousand airports, twenty million miles of roads, seven hundred thousand miles of train tracks, and hundreds of thousands of ships and boats in the oceans at all times.

  The connectivity revolution we’ve experienced has fundamentally changed the ways that animal and human microbes move around our planet. It has radically increased the speed at which microbes can travel. It has brought populations together, allowing agents that couldn’t previously sustain themselves with low population numbers to flourish.

  As we’ll see in chapter 8, it has also permitted completely novel diseases to emerge and frightening animal viruses to extend their ranges. These technologies have created a single interconnected world—a giant microbial mixing vessel for infectious agents that previously stayed separate and stayed put. The new microbial mixing vessel that our planet has become has forever altered the way in which we’ll experience epidemics. It has truly helped usher us into the pandemic age.

  7

  THE INTIMATE SPECIES

  On February 2, 1921, Englishman Arthur Evelyn Liardet went into surgery. Liardet’s symptoms were typical, but the surgery was not. At the time of the operation, Liardet was seventy-five years old and complained of decreases in his physical and mental energy. He had lost most of his hair and had developed wrinkle lines on his face. In short, he was growing old.

  Some years before that chilly day in 1921, Liardet had written to an up-and-coming Russian surgeon practicing in Paris and offered his body for a unique procedure. The surgeon, Serge Voronoff, claimed to offer nothing other than total bodily rejuvenation—the elixir of life.

  Serge Abrahamovitch Voronoff was born in Russia in 1866. At the age of eighteen, he immigrated to France, where he studied medicine under the Nobel laureate Alexis Carrel. Carrel had won his Nobel Prize in 1912 for surgical work on blood vessels as well as the new methods of transplantation of both blood vessels and whole organs. Carrel taught Voronoff surgery, undoubtedly impressing upon him the excitement of science and the potential for discovery, particularly surrounding the revolutionary new techniques of organ transplantation. In doing so, he launched the career of the young, ambitious, six-foot-four Voronoff, described in reports as magnetic and imaginative.

  Following his studies with Carrel, Voronoff worked in Egypt for the Egyptian king. Voronoff soon became fascinated with the eunuchs that were part of the king’s harem. In particular, he noted that the castration they received seemed to increase the speed at which the eunuchs aged. This observation was the beginning of Voronoff’s obsession with a surgical answer to aging. Likely inspired by the pioneering work of his mentor and the excitement of the new surgical techniques, Voronoff began to dabble in experimental transplantation. But he went beyond the techniques that his mentor had perfected. In early experiments Voronoff transplanted the testicles of a lamb into an old ram, claiming that the transplant served to thicken the ram’s wool and increase its sex drive. These early studies foreshadowed the work that would follow.

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  Some years later, on that cold February day in Paris, Liardet became one of Voronoff’s early human experiments. Before Liardet was wheeled into the operating room, a chimpanzee had been anesthetized using a specialized “anesthetizing box” developed by Voronoff. The box served to protect the te
chnicians from the massive and potentially violent male chimpanzees, who would have certainly reacted strongly to what was coming. Then Liardet was wheeled in on a gurney and placed alongside the chimpanzee. The surgeons carefully removed a testicle from the chimpanzee, cut it into thin slices, and grafted pieces onto the testes of Liardet.

  The procedure, known in its day as the monkey gland operation, would go on to become remarkably popular. By 1923 forty-three men had received testicles from nonhuman primates, and by the end of Voronoff’s career, that number reached the thousands. Although Voronoff had inherited a fortune as an heir to a vodka manufacturer, he made more money operating on many of the most important men of his day. Unverified but highly specific accounts point to Anatole France, a Nobel Prize–winning French poet as one of his patients. Less reliable rumors suggest Pablo Picasso might also have gone under Voronoff’s knife.

  Dr. Serge Voronoff (R) in his operating room. (© Bettmann / Corbis)

  But to what end? Many of Voronoff’s patients swore by the procedure. Liardet himself claimed to a New York Times reporter in 1922 that the procedure had been a huge success. He showed the reporter his strong biceps while his wife nodded knowingly by his side. Though the successes claimed by Voronoff and his patients were certainly exaggerated, the underlying logic of the procedures remains open to at least some scientific debate. Voronoff himself, as well as his procedure, eventually fell out of favor with the scientific community. By the time of his death in the early 1950s, most considered him a quack, perhaps in part because of the extremes to which he went. In the most dramatic of his experiments, he transplanted ovaries from a human woman into a female chimpanzee named Nora. He then attempted to inseminate her using human sperm!1 Yet a 1991 editorial on Voronoff in the top British medical journal The Lancet concludes with the following words: “Maybe medical research councils should fund further research on monkey glands.”