The yellow fever outbreak in Africa this year came closer to being a disaster than is widely recognized, public health experts recently disclosed. The epidemic also revealed glaring weaknesses in the emergency vaccine supply pipeline.
The first deaths in Angola were misdiagnosed as food poisoning; the global emergency vaccine stockpile was depleted before even one city was fully protected; and diagnostic laboratories were so far away that it was months before the scope of the outbreak was clear and a worldwide alarm was raised.
Ultimately, the yellow fever outbreak was halted only by a huge vaccination campaign that stretched supplies by diluting doses, and even that succeeded only because some unusual donors stepped in.
Brazil contributed 18 million doses of yellow fever vaccine — three times the amount in the emergency stockpile — to contain the African outbreak. Even South Sudan, one of the world’s poorest nations, gave up 400,000 doses intended for its children.
The outbreak, which began last December and appeared to be over as of September, went largely unnoticed because attention was focused on the Zika epidemic. Some aspects were truly frightening, experts said at the annual conference of the American Society of Tropical Medicine and Hygiene in Atlanta in mid-November.
For the first time, the virus reached Asia — a continent with no yellow fever immunity. Ultimately, however, there were only 11 cases in China, all in returnees who had been working in Africa.
“It did not get a foothold in Asia, but if it did, it would be a real nightmare,” said Dr. Axelle Ronsse, an emergency medical coordinator for Doctors Without Borders, which led the fight against yellow fever in the Democratic Republic of Congo.
After the first case was detected in Beijing, John P. Woodall, a co-founder of the disease-alert service ProMed-mail, warned that spread in Asia “could make the Ebola and Zika epidemics look like picnics in the park!”
More than 100,000 Chinese work in Africa and many, Dr. Woodall noted, come from tropical southern China where Aedes mosquitoes already spread dengue and could spread yellow fever.
Kinshasa, Congo’s capital, narrowly missed having a runaway outbreak. There were only 16 cases far from the crowded city center.
Just 50 cases, Dr. Ronsse said, would have overwhelmed her mosquito-control teams, which sprayed 325 acres of the city.
Although there were fewer than 1,000 laboratory-confirmed cases in the outbreak over all, there were more than 6,000 suspected cases and undoubtedly many more unreported.
Only about 15 percent of cases get the characteristic yellow eyes, dark urine and abdominal pain, but half of them die.
Yellow fever was one of the great scourges of the 18th and 19th centuries. Imported to the Americas from Africa with the slave trade, the mosquito-borne virus regularly killed hundreds of thousands in Latin America and the Caribbean.
From 1702 to 1822, outbreaks emptied out New York City several times as residents, banks and government offices moved north to Greenwich Village or farther in search of safety. In 1793, the fever killed a tenth of the population of Philadelphia, which was then the nation’s capital.
Since a vaccine was invented in the 1930s, it has been held in check, circulating in monkeys in Africa and the Amazon jungle. The virus regularly starts small outbreaks in remote villages, but it can cause explosive urban outbreaks when it is transmitted from forest mosquitoes to Aedes aegypti, which prefers to live among humans.
Aedes aegypti is called the yellow fever mosquito, but it also transmits Zika, dengue and other pathogens.
In December 2015, four Eritrean workers who frequented the market in Viana, a suburb of Luanda, died, as did the owner of a restaurant where they ate. Food poisoning was suspected at first.
It was not until January, after blood samples reached the Pasteur Institute in Senegal, that the fever was diagnosed. By then it was spreading fast within Luanda, a metropolitan area of almost seven million.
By February, 12 Angolan provinces were affected. Why the disease never moved south into Namibia or east into Zambia is unclear. The borders are sparsely populated, two years of drought lowered mosquito populations, and those countries do some routine vaccination.
The virus did move north into Congo, which has two port cities, Boma and Matadi, on the border with Angola. Kinshasa, a city of 10 million, is just up the Congo River and across from Brazzaville, where two million more live.
A huge population was suddenly at risk, but the emergency vaccine stockpile, administered by a committee in Geneva, then held only six million doses.
The vaccine is grown in chicken eggs for as little as $1 a dose, said Dr. Thomas P. Monath, a vaccine expert formerly with the Centers for Disease Control and Prevention.
But because profits are low, many pharmaceutical companies dropped it. In 1970, 14 private or national vaccine factories made yellow fever vaccine; now only six do, and only four sell it to the World Health Organization. The manufacturers were asked to increase production, and other countries were asked to divert their supplies.
The outbreak turned into a race between the vaccine and the mosquitoes.
The first six million doses reached Luanda by late February, and officials in Angola requested four million more. Those did not all arrive until late May.
Then Congo urgently asked for two million doses, and Uganda, which had a brief, unrelated outbreak, requested one million. With panic spreading, it was reported that one million doses had been stolen, and that forged vaccination certificates were circulating.
On April 4, the situation looked so serious that the W.H.O. director-general, Dr. Margaret Chan, visited Luanda to draw attention to the crisis. On May 19, an expert advisory committee debated declaring a global emergency like the one it had declared for Zika in February. The committee decided to hold off because the outbreak appeared to be slowing.
Then Peru reported a big yellow fever outbreak, raising worry again; but it was brought under control without outside help.
Ultimately — and luckily — it was the mosquitoes that stumbled.
Doctors Without Borders vaccinated residents of Matadi, the Congo border city. In Kinshasa, it suppressed each of the 16 known cases by spraying every nearby house with three types of pesticide: spray on indoor walls, fog outdoors, plus larvide in standing water.
By October, more than 31 million people were vaccinated — but only by diluting each dose by five to one.
“The end of the story was successful,” Dr. Sylvie Briand of the W.H.O.’s outbreaks and emergencies branch, adding, with understatement, “but it was really a logistical challenge.”
If an outbreak had started in China, the crisis might have been much greater.
Dr. Monath calculated that 160 million doses would be needed to contain it — and only if, diluted tenfold, they still worked. At full capacity, the world’s vaccine factories produce half that many in a year.