Spillover: Animal Infections and the Next Human Pandemic (65 page)

These scientists are on alert. They are our sentries. They watch the boundaries across which pathogens spill. And they are productively interconnected with one another. When the next novel virus makes its way from a chimpanzee, a bat, a mouse, a duck, or a macaque into a human, and maybe from that human into another human, and thereupon begins causing a small cluster of lethal illnesses, they will see it—we hope they will, anyway—and raise the alarm.

Whatever happens after that will depend on science, politics, social mores, public opinion, public will, and other forms of human behavior. It will depend on how we citizens respond.

So before we respond, either calmly or hysterically, either intelligently or doltishly, we should understand in some measure the basic outlines and dynamics of the situation. We should appreciate that these recent outbreaks of new zoonotic diseases, as well as the recurrence and spread of old ones, are part of a larger pattern, and that humanity is responsible for generating that pattern. We should recognize that they reflect things that we’re
doing
, not just things that are
happening
to
us. We should understand that, although some of the human-caused factors may seem virtually inexorable, others are within our control.

The experts have alerted us to these factors and it’s easy enough to make a list. We have increased our population to the level of 7 billion and beyond. We are well on our way toward 9 billion before our growth trend is likely to flatten. We live at high densities in many cities. We have penetrated, and we continue to penetrate, the last great forests and other wild ecosystems of the planet, disrupting the physical structures and the ecological communities of such places. We cut our way through the Congo. We cut our way through the Amazon. We cut our way through Borneo. We cut our way through Madagascar. We cut our way through New Guinea and northeastern Australia. We shake the trees, figuratively and literally, and things fall out. We kill and butcher and eat many of the wild animals found there. We settle in those places, creating villages,
work camps, towns, extractive industries, new cities. We bring in our domesticated animals, replacing the wild herbivores with livestock. We multiply our livestock as we’ve multiplied ourselves, operating huge factory-scale operations involving thousands of cattle, pigs, chickens, ducks, sheep, and goats, not to mention hundreds of bamboo rats and palm civets, all confined en masse within pens and corrals, under conditions that allow those domestics and semidomestics to acquire infectious pathogens from external sources (such as bats roosting over the pig pens), to share those infections with one another, and to provide abundant opportunities for the pathogens to evolve new forms, some of which are capable of infecting a human as well as a cow or a duck. We treat many of those stock animals with prophylactic doses of antibiotics and other drugs, intended not to cure them but to foster their weight gain and maintain their health just sufficiently for profitable sale and slaughter, and in doing that we encourage the evolution of resistant bacteria. We export and import livestock across great distances and at high speeds. We export and import other live animals, especially primates, for medical research. We export and import wild animals as exotic pets. We export and import animal skins, contraband bushmeat, and plants, some of which carry secret microbial passengers. We travel, moving between cities and continents even more quickly than our transported livestock. We stay in hotels where strangers sneeze and vomit. We eat in restaurants where the cook may have butchered a porcupine before working on our scallops. We visit monkey temples in Asia, live markets in India, picturesque villages in South America, dusty archeological sites in New Mexico, dairy towns in the Netherlands, bat caves in East Africa, racetracks in Australia—breathing the air, feeding the animals, touching things, shaking hands with the friendly locals—and then we jump on our planes and fly home. We get bitten by mosquitoes and ticks. We alter the global climate with our carbon emissions, which may in turn alter the latitudinal ranges within which those mosquitoes and ticks live. We provide an irresistible opportunity for enterprising microbes by the ubiquity and abundance of our human bodies.

Everything I’ve just mentioned is encompassed within this rubric: the ecology and evolutionary biology of zoonotic diseases. Ecological circumstance provides opportunity for spillover. Evolution seizes opportunity, explores possibilities, and helps convert spillovers to pandemics.

It’s a neat but sterile historical coincidence that the germ theories of disease came to scientific prominence at about the same time, in the late nineteenth century, as the Darwinian theory of evolution—neat because these were two great bodies of insight with much to offer each other, and sterile because their synergy was long delayed, as germ theories remained for another sixty years largely uninformed by evolutionary thinking. Ecological thinking, in its modern form, arose even later and was equally slow to be absorbed by disease science. The other absent science, until the second half of the twentieth century, was molecular biology. Medical people of the earlier eras might guess that bubonic plague was somehow related to rodents, yes, but they didn’t know how or why until Alexandre Yersin, during an 1894 epidemic in Hong Kong, found the plague bacterium in rats. Even that didn’t illuminate the path to human infection until Paul-Louis Simond, several years later, showed that the bacterium is transmitted by rat fleas. Anthrax, caused by another bacterium, was known to kill cows and people but seemed to arise by spontaneous generation until Koch proved otherwise in 1876. Rabies was even more obviously associated with transmission to humans from animals—notably, mad dogs—and Pasteur introduced a rabies vaccine in 1885, injecting a bitten boy, who survived. But rabies virus itself, so much smaller than a bacterium, couldn’t be directly detected nor traced to wild carnivores until much later. During the early twentieth century, disease scientists from the Rockefeller Foundation and other institutions conceived the ambitious goal of eradicating some infectious diseases entirely. They tried hard with yellow fever, spending millions of dollars and many years of effort, and failed. They tried with malaria, and failed. They tried later with smallpox, and succeeded. Why? The differences among those three diseases are many and complex, but probably the most crucial one is that smallpox resided neither in a reservoir host nor in a vector. Its ecology was simple. It existed in humans—in humans only—and was therefore much easier to eradicate. The campaign to eradicate polio, begun in 1988 by WHO and other institutions, is a realistic effort for the same reason: Polio isn’t zoonotic. And malaria is now targeted again. The Bill and Melinda Gates Foundation announced, in 2007, a new long-term initiative to eradicate that disease. It’s an admirable goal, a generously imaginative dream, but a person is left to wonder how Mr. and Mrs. Gates and their scientific advisers propose to deal with
Plasmodium knowlesi
. Do you exterminate the parasite by killing off its reservoir hosts, or do you somehow apply your therapeutics to those hosts, curing every macaque in the forests of Borneo?

That’s the salubrious thing about zoonotic diseases: They remind us, as St. Francis did, that we humans are inseparable from the natural world. In fact, there
is
no “natural world,” it’s a bad and artificial phrase. There is only the world. Humankind is part of that world, as are the ebolaviruses, as are the influenzas and the HIVs, as are Nipah and Hendra and SARS, as are chimpanzees and bats and palm civets and bar-headed geese, as is the next murderous virus—the one we haven’t yet detected.

I don’t say these things about the ineradicability of zoonoses to render you hopeless and depressed. Nor am I trying to be scary for the sake of scariness. The purpose of this book is not to make you more worried. The purpose of this book is to make you more smart. That’s what most distinguishes
humans from, say, tent caterpillars and gypsy moths. Unlike them, we can be pretty smart.

Greg Dwyer came around to this point during our talk in Chicago. He had studied all the famous mathematical models proposed to explain disease outbreaks in humans—Anderson and May, Kermack and McKendrick, George MacDonald, John Brownlee, and the others. He had noted the crucial effect of individual behavior on rate of transmission. He had recognized that what people do as individuals, what moths do as individuals, has a large effect on
R
0.
The transmission of HIV, for instance, Dwyer said, “depends on human behavior.” Who could argue? It has been proven. Consult the changes in rate of transmission among American gay men, among the general populace of Uganda, or among sex workers in Thailand. The transmission of SARS, Dwyer said, seems to depend much on superspreaders—and their behavior, not to mention the behavior of people around them, can be various. The mathematical ecologist’s term for variousness of behavior is “heterogeneity,” and Dwyer’s models have shown that heterogeneity of behavior, even among forest insects, let alone among humans, can be very important in damping the spread of infectious disease.

“If you hold mean transmission rate constant,” he told me, “just adding heterogeneity by itself will tend to reduce the overall infection rate.” That sounds dry. What it means is that individual effort, individual discernment, individual choice can have huge effects in averting the catastrophes that might otherwise sweep through a herd. An individual gypsy moth may inherit a slightly superior ability to avoid smears of NPV as it grazes on a leaf. An individual human may choose not to drink the palm sap, not to eat the chimpanzee, not to pen the pig beneath mango trees, not to clear the horse’s windpipe with his bare hand, not to have unprotected sex with the prostitute, not to share the needle in a shooting gallery, not to cough without covering her mouth, not to board a plane while feeling ill, or not to coop his chickens along with his ducks. “Any tiny little thing that people do,” Dwyer said, if it makes them different from one another, from the idealized standard of herd behavior, “is going to reduce infection rates.” This was after I had asked him to consider The Analogy and he had pushed his brain against it for half an hour.

“There’s only so many ways gypsy moths can differ,” he said finally. “But the number of ways that humans can differ is really, really huge. And especially in their behavior. Right. Which gets back to your question, which is, How much does it matter that humans are smart? And so, I guess I’m actually going to say that it matters a whole lot. Now that I stop to think about it carefully. I think it will matter a great deal.”

Then he took me into the basement of the building and gave me a glimpse of the experimental side of his work. He unlocked a door to what he called “the dirty room,” opened an incubator, took out a plastic container, and showed me gypsy moth caterpillars infected with NPV. I saw what it looks like to go
splat
on a leaf.

115

O
f the two giant elm trees that stood before my neighbor Susan’s house, only one remains. The other died about four years ago, senescent, drought stricken, and harried by aphids. A contract arborist came with his crew and his truck and took it down, limb by limb, section by section. That was a sad day for Susan—for me too, having lived in the shade of that majestic hardwood for almost three decades. Then even the stump, big enough to serve as a coffee table, vanished. It had been ground down with a stump grinder and covered with grass. The tree is now gone but not forgotten. The neighborhood is less graceful for its loss. But there was no choice.

The other big elm is still here, arching grandly over our little street. Circling the tree’s grayish brown bark, at waist level, is a stain—a dark band of discoloration, evidently indelible against weather and time, marking where it was defended with toxic goo against the tent caterpillars, twenty years ago. The caterpillars are long departed, just another outbreak population that crashed, but this mark is like their fossil record.

When I’m home in Montana, I walk past that tree every day. Usually I notice the dark band. Usually I remember the caterpillars, how they came in such numbers and then disappeared. Conditions had been good for them. But something happened. Maybe luck was the crucial element. Maybe circumstance. Maybe their sheer density. Maybe genetics. Maybe behavior. Often nowadays, when I see the mark on the tree, I recall what Greg Dwyer told me: It all depends.

NOTES

I. Pale Horse

24. “
Viruses have no locomotion
”: Morse (1993), ix.

28. “
He remained deeply unconscious
”: O’Sullivan et al. (1997), 93.

29. “
It seems
,
”
McCormack’s group concluded,
“
that very close contact
”: McCormack et al. (1999), 23.

35. “
Economically, it is the most important
”: Brown (2001), 239.

41. “
If you look at the world from the point of view
”: William H. McNeill, in Morse (1993), 33–34.

44. “
Furthermore, 71.8% of these zoonotic
”: Jones-Engel et al. (2008), 990.

II. Thirteen Gorillas

54. “
The chimpanzee seems to have been the index case
”: Georges et al. (1999), S70.

70. “
Only limited ecological investigations
”: Johnson et al. (1978), 272.

71. “
No more dramatic or potentially explosive epidemic
”: Johnson et al. (1978), 288.

72. “
No evidence of Ebola virus infection
”: Breman et al. (1999), S139.

77. “
Contact with nature is intimate
”: Heymann et al. (1980), 372–73.

84. “
Viruses of each species have genomes that
”: Towner et al. (2008), 1.

87. “
bad human-like spirits that cause illness
”: Hewlett and Hewlett
(2008), 6.

88.
a final “love touch” of the deceased
: Hewlett and Amola (2003), 1245.

90. “
This illness is killing everyone
”: Hewlett and Hewlett (2008), 75.

91. “
Sorcery does not kill without reason
”: Hewlett and Hewlett (2008), 75
.

92. “
jumped from bed to bed, killing patients left and right
”: Preston (1994), 68.

92. “
transforms virtually every part of the body
”: Preston (1994),
72.

92. “
suddenly deteriorates,
” its internal organs deliquescing
: Preston (1994),
75.

92. “
essentially melts down with Marburg
”
: Preston (1994),
293.

92.
comatose, motionless, and
“bleeding out”
: Preston (1994),
184.

93. “
Droplets of blood stand out on the eyelids
”
: Preston (1994),
73.

99. “
It is difficult to describe working with a horse infected with Ebola
”
:
Yaderny Kontrol
(Nuclear Control)
Digest
, No. 11, Center for Policy Studies in Russia, Summer 1999.

119. “
Taken together, our results clearly point
”
: Walsh et al. (2005), 1950.

120. “
Thus, Ebola outbreaks probably do not occur as
”
: Leroy et al. (2004), 390.

III. Everything Comes from Somewhere

132.
some interesting points about “smouldering” epidemics
:
Hamer (1906), 733–35.

132.
This idea became known as the
“mass action principle”
:
Fine (1979), 348.

133.
“
the acquisition by an organism of a high grade of infectivity
”
: Brownlee (1907), 516
.

133.
“
the condition of the germ
”
: Brownlee (1907), 517.

133.
“
extirpated once and forever
”
: Ross (1910), 313.

133.
a “theory of happenings”
: Ross (1916), 206.

134.
“
so little mathematical work should have been done
”
: Ross (1916), 204–5.

141.
“
This indicates,
” they wrote confidently, “that human
P. falciparum
”
: Liu et al. (2010), 424.

141.
“
a monophyletic lineage within the gorilla
P. falciparum
radiation
”
: Liu et al. (2010), 423.

143.
“
One of the most important problems in epidemiology
”
: Kermack and McKendrick (1927), 701.

144.
“
Small increases of the infectivity rate
”
: Kermack and McKendrick (1927), 721.

146.
“
very small changes in the essential transmission factors
”
: MacDonald (1953), 880.

146.
“
the number of infections distributed in a community
”
: MacDonald (1956), 375.

147.
“
It all but destroyed malariology
”
: Harrison (1978), 258.

151.
“
The effect was remarkable
”
: Desowitz (1993), 129.

152.
“
This occurrence,
” wrote a quartet of the doctors involved
: Chin et al. (1965), 865.

161.
“
it is possible that we are setting the stage for a switch
”
: Cox-Singh and Singh (2008), 408.

IV. Dinner at the Rat Farm

169.
“
hospitalized for treatment of severe, acute respiratory syndrome
”
: World Health Organization (2006), 257.

169.
“
During the past week,
” it said, “WHO has received reports”
: World Health Organization (2006), 259–60.

171.
described simply as
“a local government official”
: Abraham (2007), 30.

171.
labeling it “atypical pneumonia”
: Abraham (2007), 34.

172.
“
Population estimates of R
0
can obscure
”
: Lloyd-Smith et al. (2005), 355.

173.
“
Each time they began to insert the tube
”
: Abraham (2007), 37.

182.
alarming rumors about “a strange contagious disease”
: World Health Organization (2006), 5.

184.
“
The first thing going through our minds
”
: Normile (2003), 886.

185.
announcing this new coronavirus as “a possible cause”
: Peiris (2003), 1319.

186.
“
We were too cautious,
” one of them said later
: Enserink (2003), 294.

187. “
Southern Chinese have always noshed more widely
”
: Greenfeld (2006), 10.

189.
“
The animals are packed in tiny spaces
”
: Lee et al. (2004), 12.

191.
“
from another, as yet unknown, animal source
”
: Guan et al. (2003), 278.

195.
“
An infectious consignment of bats
”
: Li et al. (2005), 678.

206.
“
humankind has had a lucky escape
”
: Weiss and McLean (2004), 1139.

V. The Deer, the Parrot, and the Kid Next Door

211.
known initially as “abattoir fever”
: Sexton (1991), 93.

212.
an example of
“public hysteria” commensurate with flagellation
:
The Washington Post,
January 26, 1930, 1.

214.
“
three died in agony
”
: Van Rooyen (1955), 4.

214.
“
The year 1929 marked a turning point
”
: Van Rooyen (1955), 5.

215.
“
tall with a gnarled Lincolnian face
”
: De Kruif (1932), 178.

218.
“
If the young cockatoo, after capture
”
: Burnet and MacNamara (1936), 88.

219.
“
a distinct clinical entity
”
: Derrick (1937), 281.

219.
“
a filterable virus,
” meaning an agent so small
: Burnet and Freeman (1937), 299.

220.
“
Most significant discoveries just grow on one
”
: Burnet (1967), 1067.

220.
“
From that moment, there was no doubt
”
: Burnet (1967), 1068.

220.
“
Problems of nomenclature arose
”: Burnet (1967), 1068.

221.
“
the Nine Mile agent
”
: McDade (1990), 12.

221.
“
sharp pains in the eyeballs
”
: McDade (1990), 16.

221.
“
There is no disease to match Q fever
”
: Burnet (1967), 1068.

222.
“
One of the more bizarre episodes
”
: Burnet (1967), 1068.

223.
“
there was no drop of rain
”
: Karagiannis et al. (2009), 1289.

226.
The other was a “hobby farm”
: Karagiannis et al. (2009), 1286, 1288.

228.
“
windborne transmission
” as the most likely source
: Karagiannis et al. (2009), 1292.

231.
“
a filterable virus,” a microbe so tiny
: Burnet (1940), 19.

233.
“
I just don’t know if I can watch it
”
: Enserink (2010), 266.

234.
“
were on the whole too busy to think of anything but
”
: Burnet (1940), 2–3.

235.
“
Other workers with an appreciation of modern developments
”
: Burnet (1940), 3.

235.
“
The parasitic mode of life is essentially similar
”
: Burnet (1940), 8.

236.
“
It will be clear, however,
” Burnet wrote
: Burnet (1940), 12.

236.
“
Like many other infectious diseases, psittacosis
”
: Burnet (1940), 19.

237.
“
those cockatoos, left to a natural life in the wild
”
: Burnet (1940), 23.

237.
“
It is a conflict between man and his parasites
”
: Burnet (1940), 23.

238.
such a thing as
“chronic Lyme disease”
: Feder et al. (2007), 1422.

238.
“
No convincing biologic evidence exists
”
:
IDSA News,
Vol. 16, No. 3, Fall 2006, 2.

239.
“
post-Lyme disease syndrome
” was another matter
:
IDSA News,
Vol. 16, No. 3, Fall 2006, 1.

239.
“
by allowing individuals with financial interests
”
: Quoted in press release, Office of the Attorney General of Connecticut, May 1, 2008, 2.

239.
“
no convincing evidence for the existence
”
: Quoted in press release, IDSA (Infectious Diseases Society of America), April 22, 2010, 2.

241.
began calling the syndrome
“Lyme arthritis”
: Steere et al. (1977a), 7.

242.
were now calling
“Lyme disease”
: Steere and Malawista (1979), 730.

243.
“
a disease of the past,
” no longer justifying
: Burgdorfer (1986), 934.

244.
“
No longer did we hear, ‘get out’
”
: Burgdorfer (1986), 936.

244.
later jovially called the
“lymelight”
: Burgdorfer (1986), 936.

245.
“
Dammin’s northeastern deer ixodid
”
: Ostfeld (2011), 26.

246.
“
The notion that Lyme disease risk is closely tied
”
: Ostfeld (2011), 22.

246.
One journal article had called white-tailed deer
: Both this article and the next, quoted in Ostfeld (2011), 22.

247.
“
The higher the number of deer in an area
”
:
The Dover-Sherborn Press,
January 12, 2011.

247.
“
Any infectious disease is inherently an ecological system
”
: Ostfeld (2011), 4.

248.
“
Thus began my interest in Lyme disease ecology
”
: Ostfeld (2011), x.

249.
“
a messy and challenging task
”
: Ostfeld (2011), 48.

250.
“
exquisitely sensitive
” to chemical and physical signals
: Ostfeld (2011), 23.