The howler monkeys slink like cats through the canopy,
swiveling their heads to look for danger. They have reason to be wary. In the
jungle below, biologists armed with a black tranquilizer rifle are hunting
them, flashes of khaki through the foliage.
The scientists signal each other with snaps and
whistles and pivot directions frequently; they often cross trails
perpendicularly instead of following them. As they maneuver for clean shots,
thick leaves come rattling down through the branches. In the distance,
marmosets whistle.
The scientists are on Ilha Grande, an island off
southern Brazil that once housed a notorious maximum security prison. Resorts
dot the perimeter today, but untouched jungle dominates the interior. Brazil
recently experienced its worst outbreak of yellow fever in decades with
hundreds of cases, some just east of Ilha Grande. So scientists plan to test
local howler monkeys (called bugios) for the virus to learn whether
it has spread here, too. If they can catch one.
Suddenly, a shot—a sharp hiss. A 20-centimeter dart
with a red tuft for a tail rockets upward. The shooter is Filipe Abreu, a Ph.D.
student at the Oswaldo Cruz Foundation (Fiocruz), a research institute in Rio
de Janeiro, Brazil. Abreu looks as if he's been in the wild for weeks: muddy
pants, scruffy beard, machete dangling from his belt. He's an entomologist, but
the intricate transmission cycle of yellow fever, which involves both monkeys
and mosquitoes, compels him to study primates, too.
The shot misses. Instead of leaves, the dart comes
clattering down. A second shot also goes awry, striking a branch and bending
the needle tip 45°.
The party regroups, and Abreu hands the rifle to
Marcelo Quintela Gomes, a technician at Fiocruz. The hunters thread through
vines and shinny down trees into a gully. Every so often Gomes raises the
rifle, then drops it. He eventually takes three shots, all misses. Everyone
agrees that the bugios are unusually skittish.
They're not the only ones. Yellow fever has left the
people of Brazil feeling edgy as well. Over the past 8 months, they've endured
vaccine shortages, lurid media stories, and the occasional slaughter of
innocent monkeys. To stem such problems, scientists have scoured this massive
country to figure out where the virus lurks and how it's spreading—knowledge
vital to fighting future outbreaks as well. But fear remains, especially the
fear that yellow fever will ravage the megacities along Brazil's east coast—or
push even beyond that.
"We've seen Zika march up to the United
States," says Seth Berkley, CEO of Gavi, the Vaccine Alliance, in Geneva,
Switzerland. So have dengue fever, chikungunya, and other mosquito-borne
diseases. "There's no reason to think yellow fever won't do the
same," he says.
Yellow fever risks are high in forest clearings, where
people often live close to monkeys that may carry the virus.
Yellow fever was once the world's most feared disease.
Most victims suffer only fevers and aching joints, but 15% get walloped: Their
eyes and skin turn yellow, and they bleed from the mouth and eyes. (The Spanish
name for the disease, vomito negro, means "black vomit.")
No drugs exist to treat it, and half of those who develop the serious form die
as the virus destroys their livers.
Native to Africa, yellow fever spread to the Americas
with the slave trade. In 1793, then-President George Washington fled
Philadelphia, Pennsylvania (then the U.S. capital), during an epidemic that
killed 5000. Later outbreaks nearly derailed the construction of the Panama
Canal.
A vaccine developed in the 1930s largely eliminated
the disease in North America. Africa and South America, meanwhile, continue to
suffer. Sub-Saharan Africa accounts for 90% of cases, including a 2016 outbreak
centered in Angola with thousands of victims. But in some ways yellow fever in
South America is scarier: Because of the low natural immunity there, it kills
one-third of those who contract it.
Brazil seems particularly vulnerable. Yellow fever
long ago disappeared into the interior, and given the mere handful of cases most
years (2014 saw none at all), few people outside endemic areas get vaccines.
But in December 2016, victims began appearing in the east for the first time
since 1942. The government confirmed 792 cases in 130 cities nationwide, with
several hundred more under investigation. More than half occurred in Minas
Gerais (population: 21 million), a southeastern state bordering the states of
Rio de Janeiro (17 million) and São Paulo (44 million). One victim reportedly
died within 40 kilometers of the city of Rio.
State health ministries, which administer vaccines,
have ordered 26.3 million emergency doses since December, but some places still
ran short. During Carnival in February, a squirrel monkey died of yellow fever
in Utinga State Park in Belém in northern Brazil. After panicked stories in the
press, people stampeded vaccine clinics, which had to open extra rooms to
contain the crowds. After 12,000 inoculations in 5 days, Belém's clinics
exhausted their supply.
Although the onset of winter slowed the outbreak,
scientists fear a resurgence next year. When and where it might reappear
depends on the erratic and often maddening behavior of three animals:
mosquitoes, monkeys, and humans.
Brazil's fever year
Yellow fever is endemic in much of Brazil, but this
year cases appeared in areas not considered at risk before. Several coastal
states saw cases not far from major cities.
CREDITS: (MAP) J. YOU/SCIENCE; (GRAPHIC) K.
SUTLIFF/SCIENCE; (DATA) BRAZIL MINISTRY OF HEALTH
Two transmission cycles of yellow fever exist in South
America. In the sylvatic (jungle) cycle, mosquitoes from two genera—Sabethes and Haemagogus—spread
the virus mostly between monkeys, with people (usually loggers or miners in
remote areas) bitten and infected only incidentally. But the possibility of an
urban cycle looms. Here, a different mosquito, the infamous Aedes
aegypti, spreads the disease directly from person to person, and cases
quickly multiply. All the recent cases in Brazil have been sylvatic—a slight
misnomer because some have occurred inside cities—but no human-to-human
transmission has occurred.
Pinning down which mosquito species carry the virus
can yield clues about who is at risk and where. So on a recent June morning,
entomologists from the Evandro Chagas Institute in Belém don green jumpsuits
and drive north to the jungle. On the way, they swap stories about all the
mosquito-borne diseases they've endured. Leathery old Hélio Saraiva has had
three strains of dengue.
They park at a dilapidated banana farm and start
gathering equipment. "Just in case, bring the big knife," someone
says. Saraiva grabs a 45-centimeter machete with ENTOMOLOGIA on
the scabbard. As they head off, the farm's resident Dalmatian trots up to join
the adventure.
After several turns, they stop. Twelve meters above is
a platform—or rather, four ragged planks. Yellow fever mosquitoes dine on
monkeys in the canopy, so researchers have to scale trees, too. There's no
ladder, just a few dozen nails pounded into the trunk to hoist yourself up.
It's a drenching climb in the heat.
An ignorant reporter asks what they use for mosquito
bait. Bruna Sena Nascimento, an animated entomologist,
laughs. "We are
the bait." Oh. Mosquitoes are attracted to the carbon dioxide that primates
exhale. So unlike with monkeys, hunting mosquitoes is easy: Just sit and
wait—and hold off on the bug spray.
In the old days, researchers sometimes sat on
platforms in their underwear, counting bites and noting what parts of the body
mosquitoes preferred. Now, fully clothed scientists use short white nets to nab
mosquitoes in the air. They then slip tubes into the nets, suck the bugs up
with their lungs, and puff them out into collection vessels—anything from
sawed-off sections of PVC pipe to plastic Teenage Mutant Ninja Turtles cups
with lids. ("Entomology is a cheap science," Abreu says. "You
improvise.") A half-day in the canopy can net a few hundred skeeters.
Identifying mosquito species is labor-intensive and
done by hand.
© MAURICIO SUSIN
Bruna Sena Nascimento brings the mosquitoes she
catches in the forest back to a lab at the Evandro Chagas Institute in Belém,
Brazil.
© MAURICIO SUSIN
At the lab, she identifies the species and checks for
signs of the yellow fever virus.
© MAURICIO SUSIN
Back at the lab in Belém, Nascimento freezes and sorts
her mosquitoes, focusing on the abdominal stripes or sweeping back legs that
distinguish various species. After the sorting, the mosquitoes go into vials
filled with saline and a BB. An automatic agitator then liquefies the bugs,
producing a foamy gray ink with floating legs. The fluid is added to cell
cultures to test for yellow fever.
Although scientists know the disease's main vectors in
Brazil, they're still investigating whether others play a role. One mystery is
how outbreaks shift from sylvatic to urban and what species drive that shift.
Perhaps miners or loggers simply carry the virus back to cities. But certain
mosquitoes might play a role, too. Abreu suspects that A. albopictus,
the Asian tiger mosquito, which often straddles jungle and urban areas, might
harbor the virus and could bridge the cycles by introducing cases into new
areas.
Even the known vectors wreak plenty of havoc, though.
Says Thomas Monath, a yellow fever expert at NewLink Genetics, a biotech
company in Ames, Iowa: "In Brazil, they've drawn a line that supposedly
demarcates risk. We vaccinate people on one side and don't vaccinate people
living on the other side. But mosquitoes aren't observing that
demarcation."
If mosquitoes are the villains of yellow fever,
monkeys are the main victims. A lack of natural immunity leads to devastating
outbreaks for many South American species, especially howler monkeys. In the
throes of the disease, Abreu says, they often descend from trees to riverbanks
to slake their thirst, but lack the strength to climb up again. They end up
shivering in the dirt, wracked with pain.
During the Brazilian outbreak, health officials
nationwide asked people to report sightings of sick or dead monkeys so they
could test for yellow fever. They received reports of 5300 dead monkeys since
the outbreak started, with an unknown number related to yellow fever.
Biologists also carried out "active vigilance" campaigns, such as the
hunts on Ilha Grande.
Shooting monkeys on those hunts is only half the
challenge. After the tranquilizer hits, scientists have about 5 minutes before
the monkey passes out and plummets—during which time they're scrambling about
with a net, hoping like crazy it doesn't wander into some inaccessible area.
Once it lands safely, they check its gums, eyes, and genitals for yellow
discoloration, then take blood from the groin to test for virus. Although the
monkey usually wakes within an hour, it might remain loopy for several more,
rendering it vulnerable to falling or a jaguar attack. So scientists usually
detain it—one group uses a red dog carrier—until it recovers its wits.
Most people in Brazil know that monkeys can catch
yellow fever. Alas, many also believe that monkeys infect people, which isn't
true. (Mosquitoes do.) As a result, people in rural areas sometimes shoot
monkeys or leave poisoned fruit around, adding dozens of casualties to an
already devastating outbreak. Killing monkeys ends up harming humans as well,
says Jùlio Bicca-Marques, a primatologist at the Pontifical Catholic University
of Rio Grande do Sul in Porto Alegre, Brazil: "The death of monkeys from
yellow fever is the first warning that the virus is circulating." In other
words, monkeys are sentinels, he says, early detection systems. "Without
the monkeys in our forests, we'll be blind."
Briefly anesthetized, a monkey has its blood drawn to
check for yellow fever virus.
© MAURICIO SUSIN
Human beings, the third actor in this drama, are the
least predictable. Miners and loggers, some with fake immunization cards, jet
between sylvatic regions and cities in just hours, potentially transferring the
virus to new areas. Cutting down forests also exposes people to mosquitoes that
would otherwise remain hidden.
Building homes in forest clearings, a common practice
in Brazil, is especially risky. On one side of the road might sit shanties with
chickens wandering about and satellite dishes anchored onto mossy boulders. On
the other, a wall of thick jungle with vibrant red tropical birds and playful
monkeys. Jozelene Beckmann, who lives in Belém, home of the state park where
the squirrel monkey died, says that monkeys used to cavort along her rooftop and
slip inside her home. Unfortunately, where monkeys go, mosquitoes follow—as
does yellow fever. After years of ignoring recommendations, Beckmann finally
got vaccinated in mid-June.
Vaccinating infants for yellow fever is already
mandatory in northern and Amazonian states, where the disease is endemic, and
some scientists propose extending the law nationwide. But because vaccination
carries a small risk—one in 300,000 people develops full-blown yellow fever
after vaccination and another one in 100,000 develops meningitis—the government
has stopped short of mandating it for everyone, instead merely recommending it.
Many people in Rio and other cities ignore the recommendation. One problem is
that most vaccine clinics keep short hours, and with the Brazilian economy
struggling, people can't take time off work to visit.
The low compliance frustrates scientists because
inoculation could basically eliminate yellow fever nationwide, and do so at a
pittance. "A single dose given as an infant that costs a dollar is
effective for life. That's extraordinary," Monath says. During the Angolan
emergency last year, health officials stretched vaccine supplies with
"fractional doses" of one-fifth the normal amount, and even that
seemed to offer short-term protection.
Still, making the vaccine has its challenges. It's
hard to scale up production, for one thing, partly because many steps are still
performed by hand, the same basic way they were in the 1930s. Manufacturers
grow the virus in chicken eggs, which workers must "candle" one by
one with hand lamps to check for signs of live embryos—veins, eyes, movement.
(Dead eggs are discarded.) A single technician might examine 8000 eggs per
week. Technicians also must burn holes in the eggshells with torches to
introduce the virus, and later burn more holes around the waist of the egg to
extract the infected embryos for grinding in blenders. It's
not quite artisanal vaccine production, but it's close.
During the yellow fever outbreak this year, public
health clinics in Belém, Brazil, vaccinated hundreds of people daily.
© MAURICIO SUSIN
Another problem is more perverse: The vaccine is
almost too good at preventing yellow fever. Because it costs so little and
protects people for life, making it isn't profitable. Worldwide, just four
institutes bother, including Fiocruz. Manufacturers also dislike the uneven
market for it: low demand most years, followed by outbreaks that leave them
scrambling. Production at Fiocruz, for instance, jumped from 25 million doses
in 2016 to a planned 70 million this year—which forced the institute to cut
back severely on its vaccine for measles, mumps, and rubella.
The market could soon change, however. The World
Health Organization (WHO) recently brokered deals in several African and South
American countries to vaccinate 584 million people for yellow fever over the
next decade, with a goal of eliminating all outbreaks worldwide by 2026. That
campaign should steady the market by ensuring stable demand. To boost supply,
Fiocruz is also building a new $1 billion plant west of Rio that, in a few
years, could produce up to 100 million doses of yellow fever vaccine annually.
Still, WHO notes that production of vaccine almost
always lags behind projections. Lack of urgency among political leaders could
also weaken the campaign. "Public health authorities," says Monath,
"can basically forget about [the disease] in between these horrible
episodes." So although the new Fiocruz facility will help, eliminating
outbreaks worldwide remains an ambitious goal. The quick spread of Zika and
other mosquito-borne diseases from South America up to Texas and Florida also
suggests that yellow fever will be hard to tame.
But the danger of yellow fever in North America pales
in comparison with the disaster that could arise if it ever spread to Asia.
Even though southern Asia has all the prerequisites for yellow fever—monkeys,
mosquitoes, a warm climate—the disease has never gained a foothold on the
world's most populous continent. Perhaps, some scientists speculate, other
diseases there provide cross-immunity. Or perhaps humans have simply been
lucky. But last year, 11 Chinese men working in Angola developed yellow fever
upon returning home, the first confirmed cases in Asian history. Thankfully,
the disease spread no further. But if the urban cycle ever got established
there, 1.8 billion people—virtually all unvaccinated and presumably with high
genetic susceptibility—could be vulnerable.
Moreover, the struggle to contain yellow fever, a
familiar disease with an effective vaccine, does not augur well for our ability
to combat the new diseases that will almost certainly emerge as people push
deeper into jungles. As Jon Abramson, a pediatrician at Wake Forest University
in Winston-Salem, North Carolina, and a yellow fever adviser for WHO, puts it:
"If we can't stop outbreaks with yellow fever, we're in a lot of trouble
with other outbreaks."
In Brazil, the quest to stop the current outbreak
continues. On Ilha Grande, after the howler monkeys scatter, the hunting party
takes a break to catch insects. "Sometimes we get mosquitoes and can't get
monkeys; other times, we get monkeys but can't get mosquitoes," Abreu says
philosophically. Both are important.
But after tracking those two creatures all morning,
Abreu and Gomes now switch their attention to the final animal in the yellow
fever triad: humans. To that end, they visit the abandoned prison nearby, now a
museum.
Locals there are gossiping about a tourist who
recently found a dead monkey nearby and posted a picture on Facebook.
Unfortunately, something dragged the carcass off before authorities could test
it for yellow fever.
Abreu befriends the museum guard, whose backyard is a
popular crossing point for monkeys. She's quite taken with the tranquilizer
rifle, and he shows her how it works. Afterward they exchange contact
information, so she can alert him if she sees sick or dead monkeys. She then
asks Abreu whether it's true that monkeys give yellow fever to humans. He
assures her that they don't.
Late the next morning, Gomes finally bags a bugio,
a female. Instead of tumbling from the canopy, she slides down a thick shaft of
bamboo "like that pole the firemen come down," Abreu says. But she is
unharmed, and they get a good blood sample.
A few weeks later, the results come back: negative for
yellow fever. That's a relief—no sign yet that this ancient scourge has
infiltrated the island paradise. But with nearby mainland cities confirming
cases and tourists pouring in, it might not be long. As the rest of Brazil has
shown, exemption from yellow fever today is no guarantee of a safe tomorrow.
Sam Kean,
foto: © MAURICIO SUSIN
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