by Nathan Wolfe
The combination of factors we’ve discussed in the previous chapters has created the perfect conditions for maintaining new agents in the human species. We live in a massively interconnected world. Links made by transport networks and medical technologies radically increase the probability that an animal virus that enters into us—no matter where—will be able to gain a foothold and spread. This means that while some of the new things we’re finding might have crossed over in the past, they haven’t persisted. From our perspective, they’re new.
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On February 21, 2003, a man at the Metropole Hotel in Hong Kong was sick—very sick. He had come from the nearby Guangdong province and had arrived at the upscale hotel, which has a fitness center, restaurants, a bar, and a swimming pool. He stayed just one night in the now infamous room 911. And he would become among the most famous “super-spreaders” of modern history.
A super-spreader is a person (or animal) who plays an outsized role in the spread of an infectious disease. The resident of room 911 at the Metropole had severe acute respiratory syndrome, or SARS, and his virus spread to at least sixteen other individuals. They in turn spread the virus to hundreds of other individuals as they dispersed to the far points of the globe—Europe, Asia, North America. Even three months later, investigators were able to pull genetic information of the virus from the carpet near room 911, information that likely got there from his coughing, sneezing, or vomiting.
We do not know exactly how the resident of room 911 became infected with the SARS virus. It may have been through contact with an infected animal. We now know that SARS ultimately originated in bats. Because people in the Guangdong province commonly eat wild animals and purchase them in live animal markets, or wet markets, the resident of room 911 may have had contact with an infected bat purchased in one such market. Alternatively, he may have acquired the virus from a civet, a small carnivore and a delicacy in that region of China. By that time, civets had acquired the SARS virus from bats. Or he may have been infected from a person who had acquired the animal virus. Perhaps most likely the virus had spread undetected for some time before he got it himself.
However the Metropole guest acquired the virus, his illness appears to have sparked the SARS pandemic that would follow, a pandemic that would go on to infect thousands of people in at least thirty-two countries on every inhabited continent and have an economic impact measured in billions of dollars. The SARS pandemic provides a perfect example of how our modern world cultivates pandemics.
Hong Kong has a higher density of people living in it than almost any other city in the world and certainly higher than any city that existed prior to the twentieth century. Thousands of international flights going to just about any part of the world you can imagine originate in Hong Kong every day. It also sits a short drive from the Guangdong province of China. Guangdong houses hundreds of millions of people and its culinary history includes wild animal delicacies and dishes like pig organ soup.
The combination of high human population densities, intense livestock production, close contact with the diverse microbes of wild animals, and a massive, efficient transportation network gives us a good sense of where the world is heading with regard to pandemics. Hunters begin the process by capturing wild animals and bringing them to markets, some of which exist in highly urban areas. The wet markets, which house live animals, pose particular risks. Once an animal has been killed, the microbes within it also begin to die, but if a living wild animal makes it to one of these urban markets, the entire panoply of its microbes are placed squarely in the midst of large numbers of humans. A virus that gets out here has definitely won the microbial lottery.
While an interesting example, Guangdong is by no means unique. Regions that house important wildlife diversity are urbanizing at rapid rates throughout the entire world. Within the past few years, for the first time in human history, we became a primarily urban species—more than 50 percent of the human population now lives in urban areas, and that number is growing. By 2050 it has been estimated that 70 percent of the world’s population will live in cities. And when highly dense urban populations, the microbes of wild animal and livestock populations, and efficient transportation networks overlap, new diseases will inevitably emerge.
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In Africa the particular course of development has provided another set of unique microbial risks. In central Africa, a region where I lived and worked for a number of years, the combination of urbanization, deforestation, road building, and consumption of wild game are conspiring to create a recipe for disease emergence.
One of the most common economic activities among the Congo Basin countries is logging. Unlike the clear-cutting that characterizes logging in some parts of the world, in central Africa most logging is selective. In selective logging, roads are cut into the relatively pristine regions with valuable trees, and workers are transported into them to extract the timber.
Logging in this way has a number of consequences for how viruses emerge. Among the first things that occur when a new logging camp opens is the large influx of workers. People arrive to clear roads, cut tracks, fell trees, haul trees, cut them, load them, and manage camps; they all come together to make temporary towns. The towns consume meat, and since most of the meat consumed in rural forested regions of central Africa is from wild game, local demand for hunting increases. This attracts more hunters and incentivizes them to hunt more. All of this serves to increase the number of animals caught and, therefore, the human contact with the blood, body fluids, and corresponding microbes of the animals present in these biodiverse habitats.
Logging trucks in southern Cameroon. (Adria Prosser)
The existence of logging roads also leads to fundamental changes in the way that people can hunt. Historically, hunters lived in villages. Their daily hunting would radiate in a circular fashion from these villages, with decreased impact at the periphery of the hunting range. Logging roads provide a greater number of points at which hunters can enter the forest, lay traps, and make kills using firearms. This has been demonstrated through detailed studies in and around the Campo Ma’an National Park by the Cameroonian ecologist Germain Ngandjui. At the same time that forest access is increasing, the movement of trucks along the roads provides increased routes to urban markets, which in turn increases the number of hunters who engage in the practice.
Whether from the pressures of the workers themselves or the roads they create, the practice of logging changes the frequency at which humans have contact with wild game. The more contact that occurs, the better the chance that a new agent will jump over. This is compounded by the interconnectivity discussed in chapter 6. The villages are remote, but they are connected by road to major ports, where the logs (and microbes) can be put on ships and moved throughout the world.
Our work in some of the most rural regions in central Africa provides clear evidence that even seemingly remote places are most definitely on the grid. We regularly screen for potentially pandemic viruses like influenza, and we see evidence of the globally circulating pandemic H1N1 even in villages in the middle of the forest. And while we certainly see unusual viruses that are local, we also see cosmopolitan strains of HIV that have worked their way down the road to infect people living in distant rural lands. New agents can increasingly get in and out of even the most remote locales.
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Sometimes multiple factors accumulate to compound the emerging pandemic threats. This is exactly what’s happened with the global spread of HIV and its associated impact on the human immune system. As we’ve discussed, HIV originally entered into humans from chimpanzees almost certainly through the hunting and butchering of these animals by people in central Africa. But now that it’s in human populations, spreading and infecting such a large number of us, it has the potential to alter the emergence equation.
Among the terrible consequences of AIDS is that it hampers the immune system. In fact, when people die of AIDS, they don’t die of HIV per se. They die
because they eventually succumb to infectious diseases that their immune systems can no longer control. Approximately 1 percent of the human population worldwide is immunodeficient. While malnutrition, therapies for cancer, and organ transplantation play a role, the most significant factor is global infection with HIV.
Immunodeficiency leads to the proliferation of a whole range of usual suspects. Agents like tuberculosis and salmonella multiply more effectively in immunosuppressed people. Common agents that aren’t normally deadly can become fatal when immune systems are weak. Viruses like cytomegalovirus and human herpesvirus 8 afflict AIDS sufferers. But immunosuppression can also provide an entryway for new agents.
Most animal agents don’t come preadapted to humans. Even microbes from some of our closest relatives often require a combination of genetic changes in order to be able to survive and spread in a human host. So when a highly exposed person like a hunter contracts a new agent, the infection will generally be fleeting. Yet in an immunocompromised host, quickly evolving microbes can often gain precious time, free of immune pressure, to go through a few more generations of reproduction, increasing the probability that they will come upon the right suite of adaptations necessary to take hold in a new species.
And it doesn’t stop there. Sometimes a new virus will cross over into someone who has been exposed to an animal, but the virus will go nowhere. The existence of numerous immunosuppressed people in a community will, however, increase the chance that the virus can begin the process of spreading once it adapts to humans. Immunosuppression, as caused by HIV or another compromising agent, provides another foothold for new microbes as they cross the elusive species barrier.
This risk is not trivial. In 2007, along with my colleagues, I reported the results of a study we’d done in Cameroon to determine the rate of HIV in individuals who had contact with wild animals through hunting or butchering. We analyzed data from 191 HIV-infected people living in rural villages near forested settings. The vast majority of the individuals we studied reported butchering and consuming wild animals. Over half of the people reported butchering monkeys or apes. Most worrying, 17 of the HIV-positive individuals reported injuries while they’d hunted and butchered wild animals—perfect opportunities for direct blood-to-blood contact and bridging of blood-borne microbes.
The fact that people in direct contact with the blood and body fluids of wild animals also have HIV and may be immunocompromised represents a serious risk for the emergence of new microbes. Hunting and butchering provide opportunities for contact with the microbes present in virtually every animal tissue. When these agents are regularly in contact with people with limited defenses, it may provide a shortcut for microbes as they traverse the boundaries between species.
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Hunting and butchering create serious risks, but even contemporary industrial livestock practices, including factory farms and modern meat production, substantially alter the ways in which we interact with animals in our world. They also increase the probability that an animal virus will spill over into humans and become a pandemic.
Livestock production has changed dramatically over the past forty or so years. One of the major changes has been raw numbers (so to speak). There are now more than one billion cattle, one billion pigs, and over twenty billion chickens living on our planet. There are estimated to be more domestic animals alive today than in all the past ten thousand years of domestication through 1960 combined. Yet this is not simply a numbers game. How the animals are grown and grouped has also dramatically shifted.
In 1967 the United States had around a million pig farms. As of 2005, the number had shrunk to a little over one hundred thousand. More pigs and fewer farms means that more and more pigs are packed together on single large-scale industrial farms. The same trends exist with other livestock species. In the United States four massive companies produce over half of the cattle, pigs, and chickens. And this is not limited to the United States. More than half of the livestock produced globally now originate in industrial farm settings.
While it’s more economically efficient to grow livestock in industrial settings there are consequences for microbes. As we’ve seen with humans, larger numbers of livestock grouped more closely together increases the capacity of livestock populations to maintain novel microbes. The animals living on massive industrial farms largely do not exist in a state of perfect isolation. Contact with blood-feeding insects, rodents, birds, and bats all provide the opportunity for new agents to enter into these incredibly massive colonies of animals. When they do, the industrial farms become far more than settings to grow meat. They become incubators for infectious agents that could move into human populations. We have seen this occur with Nipah virus in Malaysian pigs, as discussed in chapter 4. Other viruses like Japanese encephalitis and influenza can act in similar ways.1
The number of livestock on the planet now boggles the mind, but the way that they’re transformed into meat also differs in important ways from how it’s been done since domestication began. Historically, a single animal would feed a family or at most a village. With the advent of processed meats, a single hot dog consumed at a baseball game can consist of multiple species (pig, turkey, cattle) and contain meat derived from hundreds of animals. When you bite into that hot dog, you’re literally biting into what was only a few decades ago an entire farm.
Combining the meat of many animals and then distributing it to many people has obvious consequences. Connecting thousands of animals with thousands of consumers means that an average meat eater today will consume bits of millions of animals during their lifetimes. What previously was a direct connection between one animal and one consumer is now a massively interconnected network of animal parts and those that eat them. And while cooking the meat certainly eliminates many of the risks, the massive number of interactions increases the potential that a rogue agent will make the jump.
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This is what appears to have happened in the case of the sheep disease scrapie and bovine spongiform encephalopathy (BSE), better known as mad cow disease. BSE is among the fascinating group of infectious agents known as prions, mentioned in chapter 1. Unlike viruses, bacteria, parasites, and any other group of life we know of on the planet, prions lack the genetic blueprints of biology (i.e., RNA and DNA). Rather than the combination of genetic material and proteins that make up all other known life, prions simply have protein. While this may seem insufficient to accomplish any organic task, prions are capable of spreading. And they can cause serious disease.
BSE was first identified as a novel cattle disease in November 1986 because of the dramatic symptoms it causes in cows. They walk and stand abnormally, and after some months they experience violent convulsions and death. While there’s still some debate about its origins in cows, it appears that it came from sheep. During the 1960s and 1970s as the development of cattle feed was industrialized, one type of cow feed involved the rendering of sheep carcasses into meat and bone meal. Sheep have long been known to have a prion disease called scrapie, and it appears that processing their carcasses as cattle feed permitted the agent to jump over and adapt.
Once it jumped to cattle, BSE then spread through more feed. Some cattle carcasses, like sheep carcasses, are also ground into feed for cattle. It appears that once the prion crossed from sheep to cattle, its primary communication was through infected cattle meat and bone meal processed for the next generation of cows.2 The spread was remarkably effective. Some have suggested that during this period more than a million infected cows may have entered into the food chain. But not all of these prions stayed in cows.
Around ten years after the first identification of BSE, physicians in the UK began to recognize a fatal neurodegenerative disease among humans who were potentially exposed to contaminated beef. The patients showed evidence of dementia, severe twitching, and an increasing deterioration of muscle coordination. Evidence from the patients’ brains revealed that they had been ravaged in exactly the same ways as those of the cow
s. Experimental evidence showed that the disease could also be transmitted to primates whose brains were inoculated with brain tissue from infected humans. These human patients had been infected with BSE, but when found in humans, the same disease is called variant Creutzfeldt-Jakob (vCJD) disease.
While only twenty-four human cases of vCJD have been confirmed to date, there are certainly others, as the definitive diagnosis is difficult to make. Much is still unknown about vCJD, but it’s increasingly suspected that infected humans must have both genetic susceptibility for the deadly brain disorder as well as exposure to infected cow tissue. Analysis of the tonsils and appendixes removed from healthy patients suggests that as many as one in four thousand people who were exposed during the UK BSE epidemic are carriers who show no sign of disease. This is particularly worrying since vCJD has been shown to pass through organ transplantation and may also pass through blood transfusions.
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The way that we now grow and distribute meat differs fundamentally from how we did it in the past. We also transport live animals in new ways. The relative ease of international shipping means that people can move livestock from regions that were once remote. And the situation is not unique to animals. Many of our plant food sources are now transported thousands of miles and eaten by millions before any microbial contamination related illness would be detected.
In chapter 6 we discussed how monkeypox rates are rising in DRC. But monkeypox has not been restricted to Africa. In 2003 monkeypox hit the United States. Careful investigation of the 2003 US outbreak showed that it emerged from a single pet store—Phil’s Pocket Pets of Villa Park, Illinois. On April 9 of that year, around eight hundred rodents representing nine different species were shipped from Ghana to Texas. The shipment included six different groups of African rodents, including Gambian giant rats, brush-tailed porcupines, and multiple species of mice and squirrel. Subsequent testing by the CDC showed that Gambian giant rats, dormice, and rope squirrels from the shipment were all infected with monkeypox, which likely spread among the animals during shipment. Some of the infected Gambian rats ended up in close proximity to prairie dogs at the Illinois pet store, and those prairie dogs appear to have seeded the human outbreak.