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A War Within a War

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Science  21 Mar 2014:
Vol. 343, Issue 6177, pp. 1302-1305
DOI: 10.1126/science.343.6177.1302

Fighting a major polio outbreak in the midst of Syria's bitter civil war is a test of commitment—and diplomacy.

Bitter medicine.

A young Syrian refugee is vaccinated against polio at Za'atari camp in Jordan.

CREDIT: SALAH MALKAWI

ZA'ATARI REFUGEE CAMP AND AMMAN—Za'atari, sometimes called Jordan's fourth largest city, was thrown together in the desert in a few months' time in 2012. This sprawling, dusty expanse of low-slung tents and prefab housing, 15 kilometers from the Syrian border, has 11 clinics, two schools, and a police station. On its bustling main thoroughfare, dubbed the Champs-Élysées, you can buy fresh fruit and vegetables, mobile phones, electric heaters, canned goods, and cigarettes; bright pink wedding dresses are on display, for sale or rent. Za'atari is now home to at least 100,000 refugees who have fled Syria's brutal civil war, more than half of them children.

Some children arrive sick and severely malnourished. Many have witnessed horrors in the course of the war, which has killed an estimated 140,000 people and displaced 8 million or 9 million. Ripped from their homes and routines, some have seen close family members taken, shot, or killed either in their towns or on the long, dangerous walk to the border. Crammed into tents or prefab trailers with their extended families, with no running water and hand-dug latrines that overflow with the rain, these children are at risk for diarrhea, respiratory disease, hepatitis A, and measles. Scabies and lice are huge problems.

And now they face the threat of polio, which erupted in Syria last October after a 15-year absence and has already paralyzed at least 37 kids—exact numbers are contentious—mostly in the opposition-held north.

"It's an emergency within an emergency," says Australian polio expert Chris Maher—not just for Syria, where millions of kids are at risk, but for surrounding countries as well, including Jordan, Lebanon, and Iraq, as refugees pour across their borders. And it's another blow to the Global Polio Eradication Initiative (GPEI), a partnership of international agencies that after 25 years has managed to chase the virus out of all but three endemic countries—Pakistan, Afghanistan, and Nigeria—but last year was hit by new outbreaks in the Horn of Africa and now Syria.

That's why Maher, who is 53 and has been fighting polio for more than 20 years, is in nearby Amman leading the biggest polio outbreak response ever attempted in the Middle East. It aims to vaccinate 23 million kids in seven countries, including wartorn Syria, repeatedly over 6 to 8 months and maybe longer. Doing so will involve tens of thousands of vaccinators delivering almost 100 million doses of vaccine. "Anything less and the virus will come and bite you on the ass," says Maher, a senior adviser on polio at the World Health Organization (WHO) in Geneva, Switzerland.

The current crisis is "one of the most challenging and visible outbreaks the Global Polio Eradication Initiative has tackled since its launch 25 years ago," wrote Bruce Aylward, a Canadian epidemiologist and physician who leads GPEI from Geneva, and Ala Alwan, WHO's regional director for the Eastern Mediterranean, in a recent article in The Lancet.

Tens of thousands of children are trapped in besieged areas, cut off from any humanitarian intervention, including polio drops. The millions of people on the move, both in Syria and the surrounding countries, are off the map and often out of reach of vaccinators. Fine-grained population mapping, precision vaccination campaigns, and monitoring—the backbone of the eradication initiative—are out of the question.

WHO and other U.N. agencies are walking the finest of lines in Syria, bound by the rules of the Assad regime but determined to vaccinate children in areas where the regime cannot go. Critics have blasted WHO for colluding with the government, vastly underestimating the size of the outbreak, and generally failing the children in the opposition-held north.

So far the response has been far from perfect. "We've made millions of mistakes," Maher says. But still, he adds, "in polio we are now reaching more people in a shorter period of time with an intervention than anyone else has succeeded in doing throughout the whole Syrian crisis"—some 3 million kids so far, each vaccinated multiple times. "And if we can create access for a polio campaign, we can create access for other humanitarian interventions."

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On an unusually warm day in January—the snow has just melted—Mohammad Mansour greets me and a translator outside his trailer and invites us in for tea. Mansour, 24, is one of the community health workers in Za'atari who goes tent to tent every month to deliver two drops of oral polio vaccine (OPV) to all children under age 5. He was a nurse in Syria before he and his family fled and landed in Za'atari more than a year ago.

Sitting cross-legged on the carpet, Mansour talks about his life back home and how it, and the country, collapsed. Health care was excellent and affordable and routine immunization rates were high, he says. But with the conflict, "everything stopped." Hospitals and clinics were destroyed and health care workers targeted—Mansour says he feared for his life. Vaccines, once plentiful, were no longer available in towns in Dara, a southern governorate where many of the refugees at Za'atari are from. The only way to get vaccine was to make a dangerous trip to a bigger city. "People decided vaccination was not worth risking their lives," Mansour says.

And now, 15 years after polio was eliminated in Syria, it is back. On 11 October, WHO got word of a cluster of 22 cases of acute flaccid paralysis, or AFP, in Deir al-Zour, a heavily contested governorate in northeastern Syria. Even before conclusive data were in, Aylward, the GPEI director, knew it was polio: The sudden, one-sided paralysis and the geographic clustering "ticked all the boxes," he told me at the time. WHO issued a global alert on 19 October warning of a suspected polio outbreak in Syria with a very high risk of spread across the Middle East. The first documented case had actually occurred on 14 July in Aleppo, but WHO only learned of it in October, after the cluster was reported. The Syrian government did not announce the outbreak until 29 October.

CREDIT: ADAPTED FROM WHO/ESRI/USGS/NOAA

The virus turned out to be closely related to two known strains, one detected in the sewers in Egypt in late 2012 and the other in Israel in early 2013. No cases have occurred in either country. Both of those strains were quickly traced back to Pakistan. The most recent genetic analyses suggest the virus may have arrived in Syria from Pakistan sometime earlier in 2012, then spread across the country and spilled across its borders, says Mark Pallansch, who heads the division of viral diseases at the U.S. Centers for Disease Control and Prevention (CDC) in Atlanta. But that remains a hypothesis, he emphasizes. (CDC, WHO, the United Nations Children's Fund [UNICEF], Rotary International, and the Bill & Melinda Gates Foundation coordinate the global eradication drive.)

Five days after issuing its initial alert, and before the Syrian government confirmed the outbreak, WHO, in collaboration with UNICEF and the Syrian Ministry of Health, began vaccinating against polio as part of an already-planned immunization campaign against measles, mumps, and rubella. "It wasn't a great campaign but it probably wasn't a terrible campaign either," Maher says. At about the same time, Jordan and other countries strengthened their border vaccination, and the first polio campaign was conducted in Za'atari on 28 October.

A beautiful plan

On 26 October, Mike Ryan was in Dublin, where he teaches international public health at University College Dublin, when he got a phone call from an old friend from WHO. It looked like there was a polio outbreak in Syria, Bruce Aylward told him. WHO needed him urgently in Amman to draw up an emergency response plan for the entire region.

"I couldn't say 'No,' " Ryan says. "Bruce and I grew up together as kids at WHO in the '90s," says Ryan, a gregarious, red-haired Irishman who led WHO's global outbreak alert and response network for more than a decade before leaving WHO in 2011. "Two days later I was on a plane to Muscat," in Oman, where on 29 October WHO's Alwan had convened the yearly meeting of all the ministers of health for the Eastern Mediterranean region. The Syrian minister was there, and polio was at the top of the agenda.

Aylward led the polio discussion. A slim, intense man with a shock of sandy hair, Aylward, 50, speaks fast and emphatically. With routine immunization falling below 50%, down from 95% or so before the war, Syria is a polio tinderbox, and several of the surrounding countries—in particular Lebanon and Iraq—do not have strong firewalls. We are dealing with a reinfection of the Middle East, Aylward told the ministers, and whatever their differences, they would have to work together to stop the outbreak.

Long walk.

In January, vaccinators got into the rebel-held areas in the north of Syria.

CREDIT: ASSISTANCE COORDINATION UNIT

To reach all children under age 5 in Syria and across the region, each country would need thousands of vaccinators to go door to door. They would need to quickly license a newer vaccine, bivalent OPV, which works against the two remaining strains of polio and is more effective than the trivalent version the countries relied on when they first wiped out the virus. And not only would the Syrian government have to commit to vaccinating every child in the country—and that meant children in opposition-held areas as well—it would have to do it six times over the next 6 months.

There were a lot of deep breaths and some equivocation, Aylward says, "but no outright 'No's.' " On 30 October, the ministers adopted a resolution declaring polio a regional public health emergency.

"The next day I flew back to Ireland and grabbed another bag and went to Amman for 5 weeks," says Ryan, where he set up WHO's one-man polio shop.

The first job was to get the warring factions to cooperate. "The concept that really rang true with all sides of the conflict was that these were children under age 2 who were being paralyzed, who have no part in any conflict. … Without taking sides we were able to articulate the view that there is one thing that could be done, and this could be done quickly and this could be done effectively."

By 26 November, Ryan, working closely with UNICEF, various nongovernmental organizations (NGOs), and ministries of health from different countries, had a draft emergency response plan for Syria, Iraq, Jordan, Lebanon, Turkey, the West Bank and Gaza Strip, and Egypt, giving top priority to Syria. Estimated to cost $40 million in its first phase, the plan clearly lays out what all of the countries would have to do over the next 6 months to a year.

But reality proved a lot messier. "It is one thing to have a beautiful plan on paper, but it is different when you are fighting a war," says Ryan, who returned to Dublin on 3 December. "It is not pretty."

Political minefield

Blunt, with short gray hair and hooded blue eyes, Chris Maher has a reputation for getting things done. When he arrived in Amman in November to relieve Ryan, he walked into a political minefield.

The Syrian regime had laid down two red lines. First, the government would allow vaccine to move "cross line" or into rebel-held or contested areas. But no vaccine could come "cross border" from another country. (Turkey, which is aligned with the opposition, was a particular flash point.)

Second, the Syrian government would retain sole authority of the outbreak response. And that meant no collaboration with the opposition or with humanitarian groups that support it, such as the Assistance Coordination Unit (ACU) or the Syrian American Medical Society (SAMS).

U.N. agencies, which operate in Syria by invitation of the government, are bound by those rules. "We are not some independent agency that can waltz in and do what we like," Maher says. But there's a problem, he adds. "Cross line has not been working in many of the contested areas."

One challenge has been getting vaccine into the besieged areas, whether they are besieged by the government or the opposition. Another is ensuring that vaccine reaches all the areas of the north where the radical Islamic State of Iraq and the Levant, known as ISIS, and more moderate opposition factions are fighting each other. Even in areas where the conflict is less intense, the lines of political control are constantly shifting, so it is hard to know who is in charge and which NGOs might be able to get in, Maher says. "If there is a bloke with a gun in your face, you don't go."

Into the north

It doesn't look like a $40 million operation. At WHO's polio command center in Amman in mid-January, the phones aren't working. Maps of Syria are taped to the walls, and the skeleton crew, several of whom have just arrived, are sharing desks. Chairs are in short supply, and the atmosphere is one of controlled chaos.

At 9 a.m., Maher is huddled over a laptop with a colleague who flew in the night before with fresh data on the January immunization round in Syria. Maher wants just one uninterrupted hour with him to figure out how many kids were vaccinated, how many were missed, where, and what needs fixing for the February round. The interruptions are constant. "Sorry about that, mate," he says after each, grumbling, "I desperately need a technical person." Maher and his colleague finally reconnect later that night and finish reviewing the data and planning the next round over a bottle of whiskey in Maher's room.

The next evening in the lobby bar in the Amman Marriott, the team's home away from home, Maher is fairly upbeat. The January rounds went better than expected, and for the first time vaccinators gained wide access across the opposition-held north. Turkey broke the logjam, supplying vaccine to the north in defiance of the Syrian regime, the humanitarian groups ACU and SAMS have just announced. Some 8500 well-trained vaccinators from local communities went door to door, delivering vaccine and marking every child's little finger to show they were vaccinated, says a SAMS staffer from the Turkey office who declines to be identified. An estimated 1.4 million kids in the north who had not been reached before were vaccinated, he says in an e-mail.

On a tightrope.

Chris Maher (top), Bruce Aylward, and Mike Ryan (shown in 2003) are treading carefully as they fight polio in Syria and the Middle East.

CREDITS (TOP TO BOTTOM): SALAH MALKAWI; U.N. PHOTO/JEAN-MARC FERRÉ; DONALD STAMPFLI/AP PHOTO

"Now we have a mechanism to get to these communities, and the mechanism is working," Maher says. "With the January round we can say with some confidence that every governorate in the country had immunization activity, and while we may not have reached every community, an awful lot of kids got immunized … maybe 80% or plus kids got immunized in January, which is bloody good."

The critics

But by dancing with the Assad regime, WHO has opened itself up to criticism. Almost from the outset, NGOs complained that WHO wasn't doing enough to reach the kids in opposition-held areas.

The accusations escalated in November and December, following articles in the German newspaper Der Spiegel and by the news agency Reuters. The news stories contended that WHO and the Syrian Ministry of Health excluded the rebel stronghold Deir al-Zour from a polio vaccination campaign in December 2012, thereby contributing to the outbreak that began there 10 months later, and that WHO was slow in testing stool samples and confirming suspected cases from rebel-held areas.

The polio outbreak in Syria was both "predictable and preventable," wrote Adam Coutts and Fouad M. Fouad, of the London School of Hygiene & Tropical Medicine and the American University of Beirut, respectively, in a 1 January opinion piece in The New York Times. Asking "why the international community did not prepare better for this eventuality," they conclude: "A disturbing part of the answer is that the United Nations itself has aggravated the situation" by ignoring Syria's larger health crisis.

Annie Sparrow, a pediatrician and assistant professor of global health at the Icahn School of Medicine at Mount Sinai in New York City, went further in a 20 February piece in The New York Review of Books titled "Syria's Polio Epidemic: The Suppressed Truth." She says that by going along with the government, WHO is significantly underestimating the size of the outbreak. In an interview, she puts the current number of cases at 100 "at a minimum," compared with WHO's 37, and says that WHO's long-established practice of defining a polio case by laboratory confirmation is "totally inappropriate" in the midst of a war. The long delay in confirming the July case from Aleppo was "absurd," she adds. If WHO had "been on the ball," she says, it would have picked up the outbreak earlier and, in its key role in GPEI, defied the regime and launched an emergency response across the entire country.

In interviews and written responses, Aylward and Alwan bristle at the notion that WHO in any way contributed to the outbreak, noting that WHO had supported the Syrian Ministry of Health in conducting preventive polio vaccination campaigns since 2010. As for omitting Deir al-Zour in the December 2012 round, Aylward snaps: "WHO doesn't make decisions about who gets vaccinated where. These are national decisions by governments." In December, violence had flared in Deir al-Zour, so the round was postponed, he says. "And Deir was covered a month later in January [2013]. They always drop that point," he adds.

Aylward concedes the organization has been in a bind because the Syrian government has so far refused to recognize any test results that are not confirmed by its own lab in Damascus or affiliated labs in Cairo and Tunis. Samples from opposition-held areas have gone an unapproved route to an accredited lab in Turkey and so are not counted on the country's official "line list." "Do we like it? No," says Aylward, who adds that WHO is in "frank discussions" with the government about the policy. Meanwhile, he says, WHO reports lab-confirmed cases from any source and continues to use all information in planning its response.

Aylward says the child paralyzed in Aleppo in July was to the best of his knowledge the first documented case, and there was nothing nefarious in the delay in confirming it. The country had been polio-free for so long that no one expected the disease. He adds: "We are $10 billion and 25 years into this [trying to eradicate polio]. Do you think we would really not vaccinate kids? Come on."

Surveillance systems are so shattered that WHO is undoubtedly missing cases, Aylward concedes. But still, he adds, even if WHO is missing half of the cases, it looks like the Syria outbreak may not be as explosive as feared. "Maybe this time we got out ahead of the virus," Aylward says, although he admits the virus could surprise them yet.

So far four campaigns have been conducted in Syria—three got into the north—and several more are planned. Some 23 million kids across the entire region have been vaccinated multiple times. If the virus doesn't spread out of Syria, the surrounding countries may stop emergency vaccination campaigns after the March to April rounds.

Maher thinks they can quash the epidemic by June, at which point he can go back to worrying about the endemic countries such as Pakistan, which spark these outbreaks in the first place. "Provided we can keep getting into the north and the fighting doesn't screw things up, we've got a shot at controlling this in the next few months."

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