World Cup raises epidemic questions

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World Cup raises epidemic questions
Panoramic photograph of crowded stadium at night
Football action at Cape Town, South Africa, during the 2010 World Cup. Do “mass gatherings” for sports and religion spread disease?
June, 2010, Damien du Toit

As international visitors prepare to visit Brazil for football’s World Cup, here’s a bummer worth worrying about: how many of them will catch dengue (DEN-gay) fever? Caused by a mosquito-borne virus, “breakbone fever” has sickened about 7 million Brazilians since 2000.

The World Cup starts June 12, runs in a dozen cities, and winds up in Rio de Janiero on July 13. Brazil had a world-record 1.4 million dengue cases last year, and some visitors inevitably will catch it during the football frenzy.

Epidemiologists consider the World Cup a “mass gathering,” an assemblage defined as 25,000 people in close contact for some period. Mass gatherings are common in sports (think world football, U.S. football and the Olympics) and religion. More than 2 million Muslims visit the Hajj, the annual pilgrimage to Mecca, Saudi Arabia.

Photo of an old newspaper headline: “Polio forces cancellation of two games”
Restrictions on gatherings have long been used to prevent infection and control epidemics. In 1952, an American college football game was canceled due to polio scare in North Carolina.

From an epidemic viewpoint, these events raise three related hazards: Visitors will

import disease to their destination

catch infections unknown by their immune systems

bring those pathogens back to their homes, spreading the epidemic

Obviously, large assemblages of strangers can effectively share infections, but what do we actually know about disease at mass gatherings — and among smaller groups of strangers on cruise ships or airliners?

Safety and the World Cup

Dengue causes a nasty fever with severe pain in the joints; a rare variant, called dengue hemorrhagic fever, can be fatal. Dengue, like every infectious disease, has its own characteristics of transmission. Unlike influenza, dengue is not spread through the air. Like many tropical diseases, it is spread by mosquitos, and that means the risk is strongly affected by weather — and the presence of small amounts of stagnant water where mosquitoes can breed.

“Dengue epidemics depend on large numbers of mosquitoes, a susceptible human population, and high rates of contact between mosquitoes and humans,” according to Rachel Lowe, at the Catalan Institute of Climate Science, in Barcelona, Spain. Lowe has just completed an innovative study1 of dengue risk at the 12 Cup locations in Brazil.

By email, Lowe wrote, “Dengue is widespread across Brazil thanks to the tropical and sub-tropical climate which allows mosquitoes to thrive during wet, warm and humid months, particularly in densely populated urban areas. Dengue is endemic in the country and transmission is never interrupted in large and warm cities, even during the southern-hemisphere winter.”

Photograph taken from behind soccer goal as a goalie dives away from a penalty shot.
In 2009, Ukrainian forward Andriy Shevchenko missed a penalty shot during a World Cup qualifying match between Ukraine and England.

  Temperature governs how mosquitoes transmit dengue between people and varies among the 12 Cup sites, notes Gerardo Chowell of the School of Human Evolution and Social Change at Arizona State University. “Small variations in temperature could mean that the vector is not yet ready to infect another individual.”

After a mosquito bites an infected person, the virus must reproduce and mature before the mosquito can infect somebody else. Depending on temperature, this “incubation period” can last from four to 10 days, so temperature “could mean a lot of variation in the size and probability of outbreaks,” Chowell explains. “Brazil has a wide range of latitude, and some cities will have outbreaks, but they will not take place in others.”

Temperature was a key input to the forecast that Lowe and colleagues used to anticipate dengue during the World Cup.

2-D world map; colors show prevalence of dengue fever; almost all in tropics
Dengue has emerged as a pandemic since the 1950s. Breakbone fever is concentrated in tropical regions with the Aedes mosquito, the dengue virus vector.

The study predicted the greatest dengue hazard in three Atlantic-coast cities — Recife, Portaleza and Natal. The safest cities include Sao Paulo and Brasilia. Rio de Janiero and Manaus occupy a middle ground.

The climate-focused study of dengue marks a new approach to public health, Lowe wrote to us. “To our knowledge this is the first example of a climate-informed dengue early warning ahead of a major global event.”

Brazil vs. dengue: an old battle

Brazil already has a national dengue program using house-to-house visits to eliminate mosquito hatcheries in standing water, such as plant pots, bottle tops and discarded tires.

In preparation for the World Cup, Lowe says, “the Brazilian Ministry of Health revised contingency plans for the host cities and states. Financial resources were increased to reduce mosquito populations and a multi-lingual information campaign was launched to inform visitors how to protect themselves from dengue.”

With dengue so well established in Brazil, cases are inevitable among the half-million international visitors. Many who come from outside the tropics are unlikely to have previous exposure to dengue, and so will lack any immune protection.

International visitors are expected to protect themselves at the World Cup. “If you have the extra cash to go to Brazil to enjoy yourself, you probably know that long sleeves and mosquito repellent are useful,” says Ajay Sethi, associate professor of population health sciences at the University of Wisconsin-Madison School of Medicine and Public Health. “If they have enough money to visit the Cup, they likely can afford good medical care. If you get vaccinated [for other diseases; dengue has no vaccine], the travel doctor will explain that, so you could avoid dengue altogether.”

Sign painted on a wall in Spanish next to a painting of a house
Public health campaign in Encarnación, Paraguay describes how to reduce outbreaks of dengue and yellow fever, another mosquito-borne virus. Headline: “Fight against all dengue and yellow fever.”
July 10, 2007, Pablo D. Flores

The final danger is that mass-gathering visitors will bring a new disease home, spreading it through the world in a “jet-plane” effect. However,

Cup fans will only spread dengue infections to places with the vector mosquito

Relatively few visitors will return to countries with significant numbers of Aedes mosquitoes/p>

Regions that do have Aedes may already have dengue, so many residents have at least partial immunity

These circumstances reduce the risk posed by returning football fans who carry the dengue virus.

The grand-daddy of mass gatherings

Aerial view of millions of visitors packed together in mosque and dressed in white with crowded cityscape in background
During Hajj, millions of pilgrims enter al-Haram Mosque and the sacred cuboid structure known as the Ka’aba. Islamic doctrine requires every able-bodied Muslim to visit the site at least once, and circumambulate the Ka’aba seven times.
December 4, 2008, Al Jazeera English

This concern about epidemics at mass gatherings is old news at the Hajj, an annual pilgrimage of Muslims from around the world to Saudi Arabia. According to one review2, “For about 1,400 years, the mass gathering at Hajj has been associated with the risk of communicable diseases, particularly respiratory infection. This risk is increased by travel (for some long and arduous), severe crowding at Hajj, the weather and the stress of Hajj rituals.”

That review noted that between 6 percent and 38 percent of Hajj visitors had influenza in various years.

In 2000, bacterial meningitis broke out at Mecca, and scientists later found that up to 80 percent of Hajj pilgrims carry this brain infection. Although they have no symptoms, they can infect pilgrims who have never been exposed to the pathogen3. After the outbreak, Saudi Arabian authorities began requiring vaccinations for pilgrims, and the number of cases per 100,000 visitors fell by 70 percent.

Cruise line chaos

Having read the horror stories of cruise ships stricken with the puke-a-minute norovirus, we began to wonder: Are cruise ships salt-water pleasure-palaces — or floating fermenters of pathogens?

Maybe not. In a 2014 review covering surveys of 6.9 million package-vacation travelers, cruisers were healthier than land travelers. Between 2000 and 2008, the overall rate of stomach upset:

* fell among cruise-ship travelers from 7 percent to 3 percent

* rose among land travelers from 6 percent to more than 9 percent

When land and sea travelers were grouped, stomach ailments appeared most often during travel to Egypt, Turkey and the Dominican Republic. That, the researchers reported, “reinforces the message that to improve traveller’s health, the sanitation and health within destination countries must be improved.”

Stomach upsets: cruise vs. land travel

Graph shows change in reported stomach upsets from 2000 to 2008 for land- and cruise-based vacations with linear trendlines
As rates of stomach upsets have fallen on cruise ships, they have risen among land-based package tours.

Getting there can be dangerous, too!

Airplanes cram passengers into confined spaces and seem ideal for transmitting viral diseases like influenza and measles, which are spread by contaminated droplets in the air. Are they? One study5 looked at passengers seated within two rows of a person with active measles. Nine of these “passenger-contacts” acquired measles, but 943 did not, for a rate of less than 1 percent.

Travellers who were vaccinated had lower odds of catching measles, as did those on a plane carrying only one case of measles.

However, a 2012 study6 of the same issue found some travelers as far as 17 rows from the active case were getting measles on airplanes, suggesting the need to search more broadly for secondary cases.

Photo of passengers in double-aisled airplane cabin; cabin about two-thirds full
Air Canada’s 777-300ER can carry 385 to 550 passengers. This may look like a flying disease incubator, but frequent air changes and heavy-duty filtering keep the air safer than it seems.

Yet before you picture a plane as a mixing bowl for airborne illness, remember that the disease may have spread during security screening, boarding or baggage claim.

Figuring it out

After searching for studies on the epidemiology of mass gatherings and transportation, we were surprised not to see many reports of illness. One possible reason: significant outbreaks may not be detected, because it’s not easy to spot disease at a mass gathering.

During epidemics, some governments try to reduce disease transmission by screening for feverish travelers at airports with infra-red scanners. “There is no proof that these work,” says Sethi, as people can be infectious before they become feverish. Nonetheless, he says screening may increase awareness. “You are educating people that something is going around, so they may change their behavior simply because they were screened.”

These events are usually brief, with many people coming and going, Chowell says. “People may get sick, but by the time they show symptoms, they are back home.”

Disease surveillance, he adds, tends to catch the worst cases but miss mild cases or people who are infected without symptoms.

If the surveillance system is working well, “I think outbreaks of a moderate size will be detected,” Chowell says, “but if surveillance is not working well, then there is a high chance that an outbreak could be missed.” Brazil, Chowell says, “has good surveillance capacity, and a large epidemic would not be missed, for sure. A dengue outbreak would be detected.”

Green Bay Packers fans celebrate an American-football touchdown against the Pittsburgh Steelers. Sports spectators attend some of the largest gatherings in the world.

The low rates of disease associated with mass gatherings, “may be surprising,” Sethi says, “but if you look at the densest cities, with 10 million population, disease may be rampant, but it’s not so high that you think of it as a disaster. At a gathering, there may not be the density of people who are susceptible.”

If vaccination or previous exposure has given the visitors or residents strong immunity, disease is likely to be limited, Sethi says, adding that other specifics also matter. “If a vector is involved, the site may not possess the vector. If the transmission is fecal to oral, like polio virus that is shed in stool, that is not going to spread as quickly as an airborne pathogen.”

Many large gatherings, Sethi notes, “involve a lot of human trafficking. At the Olympics, they distribute a massive amount of condoms for a reason.”

To understand the epidemiology of a mass gathering, Chowell says, “you need to think about the schedule of events, the locations where they take place, whether they will be closed or open spaces, the size of the spaces, the length of time people are present, and the likelihood that the pathogen could spread.”

– David J. Tenenbaum

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Kevin Barrett, project assistant; Terry Devitt, editor; S.V. Medaris, designer/illustrator; David J. Tenenbaum, feature writer


  1. Dengue outlook for the World Cup in Brazil: an early warning model framework driven by real-time seasonal climate forecasts, Rachel Lowe et al, The Lancet Infectious Diseases, Early Online Publication, 17 May 2014
  2. Prevention of influenza at Hajj: applications for mass gatherings, Elizabeth Haworth et al, J R Soc Med June 2013 vol. 106 no. 6 215-223
  3. Memish Z, et al, Laboratory-confirmed invasive meningococcal disease: effect of the Hajj vaccination policy, Saudi Arabia, 1995 to 2011. Euro Surveill.
  4. Self-Reported Stomach Upset in Travellers on Cruise-Based and Land-Based Package Holidays, Naomi J. Launders et al, PlOS ONE Jan. 2014, doi:10.1371/journal.pone.0083425.g001
  5. Measles transmission during air travel, United States, December 1, 2008–December 31, 2011, Kailey Nelson et al, Travel Medicine and Infectious Disease, Volume 11, Issue 2, March–April 2013, Pages 81-89;
  6. Patterns of measles transmission among airplane travelers, Paul J. Edelson, Travel Medicine and Infectious Disease (2012) 10, 230e235
  7. Coming soon: New machines that know exactly what’s bugging you.
  8. The Brazilian Banes: A World Cup Disease Guide
  9. In 1918 flu epidemic, timing was a Killer.
  10. World Health Organization’s Global Alert and Response (GAR) feature provides daily updates on disease outbreaks around the globe.