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REVIEW

The 2014 FIFA World Cup: Communicable


disease risks and advice for visitors to Brazil e
A review from the Latin American Society for
Travel Medicine (SLAMVI)
Viviana Gallego
a
, Griselda Berberian
a
, Susana Lloveras
a,b
,
Sergio Verbanaz
a
, Tania S.S. Chaves
c
, Tomas Orduna
b
,
Alfonso J. Rodriguez-Morales
b,d,
*
a
Panel of Sports and Travel, Latin American Society for Travel Medicine (SLAMVI), Buenos Aires,
Argentina
b
Panel of Scientic Publications and Teaching, Latin American Society for Travel Medicine (SLAMVI),
Buenos Aires, Argentina
c
Latin American Society for Travel Medicine (SLAMVI), Para, Brazil
d
Faculty of Health Sciences, Universidad Tecnologica de Pereira, Pereira, Colombia
Received 17 March 2014; received in revised form 14 April 2014; accepted 16 April 2014
KEYWORDS
Travel health;
World cup;
Infectious diseases;
Prevention;
Brazil
Summary The next FIFA World Cup will be held in Brazil in JuneeJuly 2014. Around 600,000
international visitors and participants (as well over 3 million domestic travelers) are expected.
This event will take place in twelve cities. This event poses specic challenges, given its size
and the diversity of attendees, including the potential for the transmission of imported or
endemic communicable diseases, especially those that have an increased transmission rate
as a result of close human proximity, eg, seasonal inuenza, measles but also tropical endemic
diseases. In anticipation of increased travel, a panel of experts from the Latin American Soci-
ety for Travel Medicine (SLAMVI) developed the current recommendations regarding the epide-
miology and risks of the main communicable diseases in the major potential destinations,
recommended immunizations and other preventives measures to be used as a basis for advice
for travelers and travel medicine practitioners.
Mosquito-borne infections also pose a challenge. Dengue poses a signicant risk in all states,
including the host cities. Vaccination against yellow fever is recommended except for travelers
who will only visit coastal areas. Travelers visiting high-risk areas for malaria (Amazon) should
be assessed regarding the need for chemoprophylaxis. Chikunguya fever may be a threat for
Brazil, given the presence of Aedes aegypti, vector of dengue, and the possibility of travelers
* Corresponding author. Faculty of Health Sciences, Universidad Tecnologica de Pereira, Pereira, Colombia. Tel.: 57 300 884 74 48.
E-mail addresses: arodriguezm@utp.edu.co, ajrodriguezmmd@gmail.com (A.J. Rodriguez-Morales).
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Please cite this article in press as: Gallego V, et al., The 2014 FIFA World Cup: Communicable disease risks and advice for visitors to Brazil
e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004
http://dx.doi.org/10.1016/j.tmaid.2014.04.004
1477-8939/ 2014 Elsevier Ltd. All rights reserved.
Available online at www.sciencedirect.com
ScienceDirect
j ournal homepage: www. el sevi erheal t h. com/ j ournal s/ t mi d
Travel Medicine and Infectious Disease (2014) xx, 1e11
bringing the virus with them when attending the event. Advice on the correct timing and use of
repellents and other personal protection measures is key to preventing these vector-borne in-
fections. Other important recommendations for travelers should focus on preventing water
and food-borne diseases such as hepatitis A, typhoid fever, giardiasis and travelers diarrhea.
Sexually transmitted diseases (STD) should be also mentioned and the use of condoms advo-
cated.
This review addresses pre-travel, preventive strategies to reduce the risk of acquiring
communicable diseases during a mass gathering such as the World Cup and also reviews the
spectrum of endemic infections in Brazil to facilitate the recognition and management of in-
fectious diseases in travelers returning to their countries of origin.
2014 Elsevier Ltd. All rights reserved.
Introduction
The FIFA World Cup is to be held in Brazil for the second
time in 2014 (the rst occasion was in 1950). Around
600,000 international visitors and participants (as well
over 3 million domestic travelers) are expected for the
event, which will take place in twelve cities around the
country (the largest in South America) between the 12th of
June and the 13th of July, 2014. It is a unique opportunity
for Brazil to showcase the beauty and diversity of its many
tourist attractions (including one the New Seven Wonders
of the World, Christ the Redeemer in Rio de Janeiro).
While Brazil has successfully hosted a number of large in-
ternational gatherings, this event poses specic chal-
lenges, given its size and the diversity of attendees. This
was extensively discussed at the past XVIII International
Congress for Tropical Medicine and Malaria, XLVIII Congress
of the Brazilian Society of Tropical Medicine and 3rd Latin
American Congress of Travel Medicine, which took place in
Rio de Janeiro, on September 23e27, 2012, as part of the
activities organized by the Latin American Society for
Travel Medicine (Sociedad Latinoamericana de Medicina
del Viajero, SLAMVI, http://www.slamviweb.org) [1].
There is potential for transmission of imported or endemic
communicable diseases, especially those that have an
increased transmission rate as a result of close proximity
of multiple asymptomatic but infected individuals, eg,
seasonal inuenza [2], but also tropical diseases that are
endemic in Brazil, such as malaria, dengue, leishmaniasis,
among others. In addition, such high-prole events may
also attract deliberate release of biological or other
agents, which should be also considered. For example
after the September 11, 2001 terrorist attacks in the
United States of America, preparedness and response was
raised also in international sports events, such as the Pan-
American games, which particularly included enhanced
surveillance and rapid detection of terrorist-induced or
natural outbreaks for timely intervention to limit exposure
and to implement prophylaxis [3e5]. Then, these are also
considerations that should be considered by national
health authorities in Brazil in anticipation of the FIFA
World Cup 2014.
Strategies to reduce the risk and mitigate the impact of
acquiring communicable diseases during a mass gathering
such as the World Cup and the Olympic Games, should
include pre-travel consultation, enhanced epidemic intel-
ligence to promptly detect incidents, the provision of
standard operating procedures for epidemic response, and
training and pre-accreditation of food suppliers to reduce
food-borne disease outbreaks [2]. International mass
gatherings pose specic challenges not only to imple-
menting control measures due to the mobility of the at-
tendees but also with regard to recognition and
management of infectious diseases in travelers returning to
their countries of origin. There is a huge commitment to
make the event safe for all who visit the country, including
authorities and travel medicine experts and practitioners in
Brazil [2,6e8]. Particularly, during the last three years,
then, in order to plan and prepare health system condi-
tions, particularly at the host cities, the Federal Govern-
ment of Brazil, with the joint action of the Ministry of
Health and the Ministry of Sports, installed in May 2011, the
Technical Camera of Health (Camara Tematica de Saude),
with the objective to promote interaction between
different government sectors, dene orientations, strategic
projects, responsibilities and goals to attain and also to
assess and advise the execution of preparatory actions for
the FIFA World Cup 2014 in relation to health [9]. Innovative
measures have been even taken regarding the imple-
mentation of new health strategies, for example the in-
clusion of bags with health aid devices and debrillators for
all the players [10].
In anticipation and preparation for the increased travel,
to and from Brazil, a panel of experts from the Latin
American Society for Travel Medicine (SLAMVI) developed
the current recommendations regarding the risk of the main
communicable diseases at major potential destinations,
particularly the host cities, recommended immunizations
and other preventives measures to be used as advice for
travelers and travel medicine practitioners, taking in
consideration the epidemiology of infectious diseases in the
country and its regions, states and cities. These recom-
mendations constitutes a scientic summarized version of
an already online report in Spanish of SLAMVI at its website
for healthcare professionals (http://www.slamviweb.org/
es/home/RECOMENDACIONES%20PARA%20LOS%20VIAJEROS
%20A%20LA%20COPA%20MUNDIAL%20DE%20FUTBOL%20BRA
SIL%202014.pdf) and also for travelers (http://www.
slamviweb.org/es/home/Muncial%20de%20Futbol%20Con
sejos%20para%20Viajeros%20SLAMVI.pdf).
2 V. Gallego et al.
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Please cite this article in press as: Gallego V, et al., The 2014 FIFA World Cup: Communicable disease risks and advice for visitors to Brazil
e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004
About Brazil
Brazil is the largest country in both South America and the
Latin American region. It is the Worlds fth largest coun-
try, both by geographical area and by population. It is the
largest Lusophone country in the World, and the only one in
the Americas. Bounded by the Atlantic Ocean on the east,
Brazil has a coastline of 7491 km (4655 mi) (Fig. 1). It is
bordered on the north by Venezuela, Guyana, Suriname and
the French overseas region of French Guiana; on the
northwest by Colombia; on the west by Bolivia and Peru; on
the southwest by Argentina and Paraguay and on the south
by Uruguay (Fig. 1) [11].
With a total area of 8,514,876.599 km
2
(3,287,612 sq
mi), including 55,455 km
2
(21,411 sq mi) of water, Brazil
spans three time zones (from UTC-4 in the western states,
to UTC-3 in the eastern states (and the ofcial time of
Brazil) and UTC-2 in the Atlantic islands). Brazil is the only
country in the World that lies on the equator while having
contiguous territory outside the tropics. Brazilian topog-
raphy is also diverse and includes hills, mountains, plains,
highlands, and scrublands. Much of the terrain lies between
200 m (660 ft) and 800 m (2600 ft) in elevation. The main
upland area occupies most of the southern half of the
country. The northwestern parts of the plateau consist of
broad, rolling terrain broken by low, rounded hills [11,12].
Brazil is a federation composed of 26 States in 5 ve
geopolitical regions (north, northeast, central west,
southeast and south) (Fig. 1), one Federal district (which
contains the capital city, Bras lia) and Municipalities
(Fig. 1). Among those states (ST) and cities (CI), 12 of them
will be host cities (between 1 and 3 per region) for the FIFA
World Cup 2014 (Fig. 1) [12,13].
The practice of travel medicine in Brazil began in 1997.
However, there are few specialized travel medicine services
in the country. Most of them are located in the southeast
region of the country, but there are a lot of public services
specialized in tropical, parasitic and infectious diseases,
available to attend those diseases in travelers [8,14,15].
Major communicable diseases in Brazil with
risk for travelers
Malaria
As a country with a large area in the tropics, includes major
zones of malaria and yellow fever transmission, among
many other tropical and vector-borne diseases [15,16].
Malaria is considered endemic in all the states of the north
region (Fig. 1) and some municipalities at west of Maranhao
(northeast region) and Mato Grosso (central west region)
(Fig. 1) (Table 1). However, number of cases has been
dramatically reduced over the last 8 years, falling from
over 600,000 cases in 2005 to less than 250,000 in 2012
(Fig. 2) [17].
Malaria in Brazil (as happens in most countries of Latin
America) is mostly due to Plasmodium vivax (around 88% of
the cases). More than 99.7% of the cases are reported in the
northern region of the country, which includes the munic-
ipalities at high risk of transmission [18]. Besides these
states, in cities such as Manaus (host city of the FIFA World
Cup 2014), malaria transmission also occurs in Boa Vista,
Macapa, Maraba, Porto Velho and Santarem. There is no
transmission in Belen, but in 2013, an outbreak occurred in
the Ananindeua metropolitan area (close to the forests).
Low risk areas include some regions surrounded by the
Atlantic Forest of Sao Paulo state (Ubatuba, Boicucanga,
Barra do Una and Juquitiba) and mountainous in Esp rito
Santo state, in summer (December until March). No trans-
mission is reported at Iguazu falls. Given the season in
which the World Cup will take place (dry season), it has
been considered that most travelers do not require
chemoprophylaxis for malaria. However travelers visiting
high risk areas (e.g. Amazon areas) should be assessed re-
gard the potential need for chemoprophylaxis. If indicated,
atovaquoneeproguanil, doxycycline or meoquine are
recommended. As in most of Latin America, Plasmodium
falciparum is resistant to chloroquine. In Brazil the rst line
Fig. 1 Map of Brazil, showing regions of the country, states (ST) and the host cities for the FIFA World Cup 2014 (in yellow stars),
as well the areas of yellow fever, malaria and dengue transmission.
The 2014 FIFA World Cup 3
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e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004
Table 1 Specic destinations (host cities and states, by country regions) and endemic infectious diseases of concern for
travelers to Brazil with recommendations for yellow fever vaccine according geographical areas.
Destination Endemic infectious diseases of concern for travelers to Brazil Recommendations of
Malaria
b
Dengue Leishmaniasis Schistosomiasis Yellow fever
vaccine
Vector avoidance
measures
Host City
Belo Horizonte No Yes No No Yes Yes
Brasilia No Yes No No Yes Yes
Cuiaba No Yes No No Yes Yes
Curitiba No No No No No Yes
Fortaleza No Yes No No No Yes
Manaus Yes Yes No No Yes Yes
Natal No Yes No No No Yes
Porto Alegre No No No No No Yes
Recife No Yes No No No Yes
Rio de Janeiro No Yes No No No Yes
Salvador No Yes No No No Yes
Sao Paulo No Yes No No No Yes
States
a
North Region
Acre Yes Yes Yes No Yes Yes
Amapa Yes Yes Yes No Yes Yes
Amazonas Yes Yes Yes No Yes Yes
Para Yes Yes Yes No Yes Yes
Rondonia Yes Yes Yes No Yes Yes
Roraima Yes Yes Yes No Yes Yes
Tocantins Yes Yes Yes No Yes Yes
Northeast Region
Alagoas No Yes Yes Yes No Yes
Bahia No Yes Yes Yes Yes, south
and west
Yes
Ceara No Yes Yes No No Yes
Maranhao Yes, west Yes Yes No Yes Yes
Para ba No Yes Yes Yes No Yes
Pernambuco No Yes Yes Yes No Yes
Piau No Yes Yes No Yes, south Yes
Rio Grande do Norte No Yes Yes Yes No Yes
Sergipe No Yes Yes Yes No Yes
Central West Region
Federal District No Yes No Yes Yes Yes
Goias No Yes No No Yes Yes
Mato Grosso Yes, some
municipalities
Yes Yes No Yes Yes
Mato Grosso do Sul No Yes No No Yes Yes
Southeast Region
Esp ritu Santo No Yes No No Yes, north Yes
Minas Gerais No Yes Yes Yes Yes Yes
Rio de Janeiro No Yes No No No Yes
Sao Paulo No Yes No No Yes, northwest Yes
South Region
Parana No No No No Yes, west Yes
Rio Grande do Sul No No No No Yes, west Yes
Santa Catarina No No No No Yes, west Yes
a
Excluding capital cities.
b
Risk areas, but currently low transmission during JuneeJuly.
4 V. Gallego et al.
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Please cite this article in press as: Gallego V, et al., The 2014 FIFA World Cup: Communicable disease risks and advice for visitors to Brazil
e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004
of treatment for P. falciparum malaria is artemether-
lumefantrine or artesunate plus meoquine. In the case
of P. vivax the recommended treatment is chloroquine plus
primaquine (7e14 days) [17]. Any traveler visiting endemic
areas (Fig. 1) and presenting with fever should be assessed
during and/or after the travel. Malaria is characterized by
fever and inuenza-like symptoms, including chills, head-
ache, myalgias, and malaise; these symptoms can occur at
intervals. Uncomplicated disease may be associated with
anemia and jaundice. In severe disease, seizures, mental
confusion, kidney failure, acute respiratory distress syn-
drome, coma, and death may occur. Malaria symptoms can
develop as early as 7 days (usually 14 days) after initial
exposure in a malaria-endemic area and as late as several
months or more after departure. Suspected or conrmed
malaria, especially P. falciparum, is a medical emergency,
requiring urgent intervention as clinical deterioration can
occur rapidly and unpredictably. [19] P. vivax infections are
characterized either by a long incubation or a long-latency
period between illness and relapse e in both cases up to
8e12 months [20,21]. Then, even in this setting, in
returning travelers with fever, malaria should be ruled out
(travelers should be informed of this possibility and
educated about the long incubation period of P. vivax ma-
laria and about need to seek care and inform the clinician
about possible malaria exposure in case symptoms indica-
tive of malaria occur). Malaria diagnostic tests are available
in all the health services in the northern region of the
country and in reference centres for infectious diseases in
teaching hospitals in others areas. In 2012, 2,325,775 ma-
laria microscopy tests were done in Brazil. Also specialized
travel medicine clinics are available in non-endemic areas
such as Sao Paulo and Rio de Janeiro [8].
Other vector-borne diseases (yellow fever, dengue,
chikungunya fever and chagas disease)
Regarding yellow fever vaccine this is recommended for all
the states and cities of north and central west regions
(Fig. 1) (Table 1), the state of Maranhao (northeastern re-
gion), Minas Gerais (southeastern region) and the southern
municipalities of Piau state (northeastern region), the
western and southern area of the state of Bahia (northeast
region), north of Espirito Santo (southeastern region),
northeastern area of Sao Paulo (southeast region) and
western areas of the states Parana, Santa Catarina and Rio
Grande do Sul (south region) (Fig. 1) (Table 1). In the period
February to April 2009, 28 human cases of yellow fever
were reported in Southwestern region of the state of Sao
Paulo, with a 39.3% case fatality rate [22]. In addition,
between September 2008 and June 2009, another outbreak
of yellow fever in previously unvaccinated populations
resulted in 21 conrmed cases with 9 deaths (43% case fa-
tality rate) in the southern state of Rio Grande do Sul [23].
All travelers visiting Iguazu falls should have a yellow fever
vaccination. This is not recommended for travelers visiting
cities such as R o de Janeiro, Sao Paulo, Salvador, Recife
and Fortaleza (Fig. 1) (Table 1). Unvaccinated individuals
traveling to areas where vaccination is recommended
should be vaccinated at least 10 days prior to travel. Public
education is needed about the risk of disease and in-
dications for vaccination, including contraindications and
precautions for persons who might be at increased risk of
severe adverse events [23].
Dengue is considered endemic at most of the states and
regions of Brazil, except for southern region states. During
2013, the incidence of disease was estimated in 731.5
cases/100,000pop, however states such as Mato Grosso
reached 3062 cases/100,000pop (30.6 cases/1000pop)
(Table 2). Major cities such as Sao Paulo and Rio de Janeiro
are also endemic. In the states of Santa Catarina, Rio
Grande do Sul and Parana (south region) disease occurs as
imported form. In addition to this, the months of June and
July are cool in the southern and southeastern region states
(Fig. 1). Daytime mosquito bite prevention using repellent
on exposed skin is highly recommended (Table 1). Accom-
modation with screens and air conditioning for prevention
of some vector borne infections will be useful in this
matter.
Chikunguya fever can be also a threat concern for Brazil,
given the presence of Aedes aegypti, vector of dengue, and
the possibility of travelers importing cases into the country
[14]. This is a real threat in view of the ongoing situation
with outbreaks of chikunguya in the Caribbean region (over
3000 cases between December 2013 and March 2014) in
French Guiana, Guadaloupe, Martinique, St. Barthelemy,
St. Martin, Anguila, Aruba, Dominica, St. Kitts & Nevis, St.
Maarten and UK Virgin Islands [24]. Thus, local surveillance
of this possibility in travelers from those areas arriving
Brazil for the World Cup should be also considered.
Thanks to a coordinated multi-country programme in the
Southern Cone countries, the transmission of Chagas dis-
ease by vectors and via blood transfusion was interrupted in
Brazil in 2006 [25]. Seroprevalences have rapidly decreased
in the last years. As a consequence, the current rates in
children aged between 0 and 5 years old is of the order of
10
5
, a clear indication that transmission, if it is occurring,
is only accidental [26,27]. However, is still currently highly
relevant in the country, because since 2005 (in Santa Cat-
arina state) reports of food-borne cases and outbreaks have
been described in Brazil, but also in other countries of Latin
America [28]. Contamination occurred when complete or
partial parts of the triatomine bugs or their Trypanosoma
Fig. 2 Evolution of the number of malaria cases reported in
Brazil, 2005e2012. (For interpretation of the references to
color in this gure legend, the reader is referred to the web
version of this article.)
The 2014 FIFA World Cup 5
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e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
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cruzi-infected feces come in contact with food and bever-
ages (eg. Ac ai, local fruit, juice; sugar cane juice) that are
undercooked, unpasteurized and/or raw. Seven to 8 out-
breaks (112 acute cases) occurred during 1965e2009 in
areas outside Amazonia, where the triatomine were under
control. In contrast, during 2000e2010, >1000 acute cases
were reported in 138 outbreaks, mainly in the Brazilian
Amazon. Of these cases, 776 (71%) have been attributed to
the ingestion of contaminated food and beverages [29]. In
the past Chagas disease was restricted to rural areas, but
now has been reported in urban areas such as Belem (Para
state) and Macapa (Amapa), and suburban such as Barcar-
ena, Abaetetuba (Para state), Pau Darco, Moju dos Cam-
pos, close to Santarem (also in Para state) (Fig. 1). Reports
of consumption of contaminated ac a palm fruit have been
consistently associated with T. cruzi infection [30,31].
Recent data from the network surveillance GeoSentinel
(1997e2013) did not found cases of Chagas disease in
returning travelers from Brazil [32], however the disease is
currently commonly described in migrant populations from
Brazil in other non-endemic countries [33]. Chagas disease
can occur also in travelers, as has been reported [34], and is
considered by the CDC Health Information for International
Travel 2014, the Yellow Book, that travelers who go to
Mexico, Central America, or South America, especially rural
areas, are at potential risk. However, the risk of Chagas
disease acquired during typical tourist travel is thought to
be quite minimal. Travelers who sleep outdoors or who stay
in poorly constructed housing are at greatest risk [35].
Given the food-borne transmission route, it is also recom-
mended to avoid undercooked, unpasteurized and/or raw
foods and beverages.
Dermatological conditions (Leishmaniasis,
Cutaneous larva migrans, Rickettsiosis)
Arthropods are a signicant cause of human skin lesions, as
people are unavoidably exposed to biting and stinging not
only in the rural, suburban environment but also in the
urban environment, so physicians and other healthcare
providers from endemic and non-endemic areas are
frequently confronted with patients having skin lesions
related to this cause [36,37]. Protective covering of skin
(e.g., shoes, clothing) is important to prevent the expo-
sure. In Brazil, leishmaniasis, as well other skin conditions
are transmitted by or caused by arthropods are commonly
seen (e.g. tungiasis, myiasis) [38e40].
Regarding cutaneous leishmaniasis, this parasitic disease
is common in rural areas, where is transmitted by the bite of
female sandies of the species Lutzomyia. In Brazil this
occurs mainly instates of the northern and northeast regions
as well as in the states Minas Gerais (southeast region) and
Mato Grosso (central west region) (Fig. 1) (Table 1). The
main etiological agents in Brazil are Leishmania brasiliensis,
Leishmania amazonensis and Leishmania guyanensis. During
2012, 23,547 cases of cutaneous leishmaniasis were re-
ported in Brazil, 10,196 in the northern region (4076 in Para),
followed by the northeastern region with 8279 cases (4244 in
Bahia). No vaccines or drugs to prevent this infection are
available. Preventive measures include reducing exposure
to sand ies by using personal protective measures. Trav-
elers should be advised to: avoid outdoor activities, espe-
cially from dusk to dawn, when sand ies generally are most
active; wear protective clothing and apply insect repellent
to exposed skin and under the edges of clothing, such as
sleeves and pant legs, according to the manufacturers in-
structions; sleep in air-conditioned or well-screened areas;
spraying the quarters with insecticide might provide some
protection. Fans or ventilators might inhibit the movement
of sand ies, which are weak iers [41].
Cutaneous larva migrans is highly frequent, also in
travelers returning from Brazil [32]. Caused by Ancylostoma
braziliensis (related to dogs and cats) and Ancylostoma
caninum (dogs), this parasitic skin infection can be ac-
quired by contact with contaminated soil or sand, eg. when
visiting some contaminated beaches. Creeping eruption
usually appears 1e5 days after skin penetration, but the
incubation period may be 1 month. Typically, a serpigi-
nous, erythematous track appears in the skin and is asso-
ciated with intense itchiness and mild swelling (Fig. 3).
Usual locations are the foot and buttocks, although any skin
surface coming in contact with contaminated soil can be
affected [42]. Thus, it is important to reduce contact with
Table 2 Dengue incidence rates (cases/100,000pop) in
Brazil by regions and states, 2011e2013.
Region and state 2011 2012 2013
North Region 752.6 257.9 301.3
Rondonia 206 207 544.4
Acre 2571.70 315.4 364.9
Amazonas 1779.20 143.9 467
Roraima 322.1 399.1 195.3
Para 253.8 207.7 117.3
Amapa 418.7 224.6 235.4
Tocantins 855.4 819.4 616.4
Northeast Region 368 413.5 273.3
Maranhao 179.1 79.3 53.4
Piau 322.6 387.7 156.5
Ceara 747.8 637.1 355.7
Rio Grande do Norte 731.4 891.5 529.6
Para ba 334.6 229.9 342.3
Pernambuco 251.2 356.1 93.6
Alagoas 285.5 888.4 295.6
Sergipe 189.9 215.9 37.9
Bahia 282.6 342 413.1
Southeast Region 449.6 308.6 1097
Minas Gerais 205.9 148.4 2044.6
Esp rito Santo 1147.60 334.3 1796.9
Rio de Janeiro 1036.80 1116.20 1303.8
Sao Paulo 278.4 69.6 511
South Region 131.4 17.2 241.2
Parana 339.3 42.6 624
Santa Catarina 2.8 1.5 5.8
Rio Grande do Sul 3.4 1.6 4
Central West Region 369.5 471.5 1806.1
Mato Grosso do Sul 347.5 367.3 3062.3
Mato Grosso 202.5 1054.70 1128.7
Goias 565.6 398.3 2233.6
Federal District 129.4 54.2 428
Brasil 400.5 303.9 731.5
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Please cite this article in press as: Gallego V, et al., The 2014 FIFA World Cup: Communicable disease risks and advice for visitors to Brazil
e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004
contaminated soil or sand by wearing shoes and protective
clothing and using barriers such as towels when seated on
the ground [42].
Rickettsial are systemic infections with frequent cuta-
neous manifestations. These are usually transmitted from
the host-animal reservoirs human through the bite of a wide
variety arthropods such as lice, eas and ticks. Rickettsial
spotted fever is known locally as Brazilian spotted fever
(BSF) or Sao Paulo fever caused by Rickettsia rickettsi. The
main vector is Amblyomma cajennense although other tick
species are capable of transmitting the bacteria. Trans-
mission occurs by the ticks bite and regurgitation of
contaminated saliva, or when the host scratches lesions
containing contaminated A. cajennense feces. The main
reservoir hosts are capybara (Hydrochaeris hydrochaeris),
horses and occasionally dogs [43]. Brazil is the country that
has the highest number of fatal cases per year, where
lethality in the state of Sao Paulo reaches values close to
30%, however vector ticks are found in other south states of
Brazil (Minas Gerais, Esp ritu Santo, Rio de Janeiro, Parana
and Santa Catarina) [44]. The risk for travelers is consid-
ered to be minimal [45,46].
Schistosomiasis
Another important tropical disease is schistosomiasis (only
due to Schistosoma mansoni) [47], which poses a risk for
travelers when swimming in contaminated rivers, canals,
streams, ponds or lakes [32,48]. Areas with signicant risk
include Bah a and Minas Gerais (Fig. 1) as well Sergipe,
Alagoas, Pernambuco, Paraiba and the state of R o Grande
do Norte and the Federal District (Table 1). Transmission
occurs largely in rural areas and not in cities. There is no
risk when visiting ocean beaches.
Sexually transmitted diseases and HIV/AIDS
Sexually transmitted diseases (STD) should be also
mentioned. Brazil reports the highest absolute number of
HIV/AIDS cases in Latin America (with over half-million peo-
ple infected), with a national incidence rate of 20.2 cases/
100.000pop for year 2012. The highest rate is reported in the
south region of the country (30.9), followed by north region
(21.0), southeast (20.1), central west region (19.5) and
northeast region (14.8) [49]. In addition, Hepatitis B, syphilis
and other bacterial STD are highly prevalent particularly in
the young, sexually active population [50]. Studies have
shown that travelers visiting Latin America, including Brazil,
engage in sexual activities that put them at risk of acquiring
STDand transmitting it, both in their home country and in the
visiting country [51e53]. Condom use should be recom-
mended for travelers with the potential to engage in sexual
relationships when visiting Brazil. On December 5, 2013,
UNAIDS launchedthecampaign: Protect thegoal. Salvador,
Bahia, was chosen to host the global campaign. The slogan of
the initiative, From Soweto to Salvador illustrates the
historical and cultural link that the city has with Africa and
highlights the continuity started in South Africa in World Cup
2010 World Cup campaign. This campaign uses the popularity
of football to show messages on HIV prevention [54].
Tuberculosis, inuenza, hantavirus and
leptospirosis
Tuberculosis incidence in Brazil is estimated in around 25
cases/100,000pop. In 2011, 70,000 new cases were re-
ported. In 2010, 4600 deaths due to tuberculosis were re-
ported. Tuberculosis is the fourth cause of death in the
country and the rst among AIDS patients [55]. Travelers
with a long stay (over 3 months) and/or those with close
contact with local people are at risk [56].
Inuenza is the most common vaccine preventable dis-
ease in travelers but only few travelers have inuenza
vaccine. In southern Brazil, AprileAugust is the inuenza
epidemic season, whereas northern Brazil has transmission
year round [57e59]. Data from 2000 to 2010 in Brazil
revealed that there were 3,291,946 visits for inuenza-like
illness; of these, 37,120 had samples collected and 6421
tested positive: 1690 (26%) inuenza A, 567 (9%) inuenza
B, 277 (4%) parainuenza 1571 (9%) parainuenza 2589 (9%)
parainuenza 3742 (12%) adenovirus, and 1985 (31%) res-
piratory syncytial virus [60].
Hantavirus is also a signicant public health problem in
Brazil. From 1993 up to 2007, more than 800 cases were
reported, in all regions, but particularly in the southern and
southeastern regions [61]. Risk for travelers is low when
visiting just urban areas, but should be considered as has
been suggested staying in suburban and rural areas,
Hantavirus should be included as one of the lung infections
acquired in the tropics [62,63]. Necromys lasiurus and
Oligoryzomys nigripes appear to be the main rodent res-
ervoirs of hantavirus in the Atlantic Forest and Cerrado
biomes of Brazil. N. lasiurus showed a wide potential dis-
tribution in Brazil, in the Cerrado, Caatinga, and Atlantic
Forest biomes. O. nigripes was reported along the Brazilian
Atlantic coast [64]. Anyone who comes into contact with
rodents that carry hantavirus is at risk of infection. Rodent
infestation in and around homes, hotels and hostels located
in suburban and rural areas would be a primary risk for
hantavirus exposure.
Fig. 3 A typical case of cutaneous larva migrans showing the
serpiginous and erythematous track in the skin.
The 2014 FIFA World Cup 7
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Please cite this article in press as: Gallego V, et al., The 2014 FIFA World Cup: Communicable disease risks and advice for visitors to Brazil
e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004
Leptospirosis is another environmental, zoonotic and
water -borne concern, given the fact that this disease is
highly endemic, reported in most states, counts for almost
20,000 cases between 2007 and 2011 [65]. The disease has
been associated with swimming, wading, kayaking, and
rafting in contaminated lakes and rivers. As such, it is a
recreational hazard for travelers who participate in outdoor
sports in addition to consuming contaminated food and
beverages [66e68].
Foodborne illnesses
Although these are infectious diseases concerns usually in
mind when travel to tropical countries, such as Brazil, other
risk should be considered. Travelers diarrhea and food-
borne diseases are highly common and prevalent [32,69]. In
addition to bacteria (such as Campylobacter, Shigella,
Salmonella) and viruses (norovirus, rotavirus, astrovirus,
hepatitis A); parasites should be considered, particularly
including Giardia intestinalis, Cryptosporidium sp,
Entamoeba histolytica, Strongyloides stercoralis, Taenia
solium and Taenia saginata. Typhoid fever is also reported
in Brazil with outbreaks reported during last decade in the
state of Sao Paulo [70]. Brucellosis, bovine tuberculosis and
listeriosis are also reported in Brazil [71]. In the past,
outbreaks of cholera have been reported in the country
[72], but currently the risk is low. Immunization is neither
required nor routinely recommended.
Recently, aiming to prevent foodborne illnesses during
the 2014 FIFA World Cup, Brazil has developed a risk-based
evaluation tool able to assess and grade Brazilian food
services in cities that will host football matches. This tool
has been used by the Brazilian sanitary surveillance ofcers
during the inspection of facilities where food services. This
has been considered an innovative preventative sanitary
action because it was created based on scientic informa-
tion, statistical calculation and on risks of foodborne dis-
eases occurrence [69].
Other tropical conditions
Finally, trauma and envenoming caused by different bites
(snakes [73], spiders, bats, cats and dogs) are also common
in Brazil, particularly those aquatic [74,75]. Travelers risk is
considered low.
Immunizations
Currently no vaccines are required by the Government of
Brazil on arrival to the country. However, as a general
suggestion, all travelers should be up-to-date on their
routine vaccines, including hepatitis A, inuenza, measles,
mumps and rubella [32], but also tetanus, diphtheria,
pertussis, pneumococcal and varicella if possible, as not all
persons would be candidates for these last two vaccines in
many countries [76]. Unfortunately, recent data of travelers
to Brazil, eg. from Boston, USA, revealed that 71%, 58%, and
50% received vaccines for yellow fever (YF), typhoid, and
hepatitis A, respectively. Fewer received inuenza and
hepatitis B vaccines (14%, 11%) [59]. Recommended vac-
cines include hepatitis A (if not included as routine vaccine
in the country of origin of the traveler), hepatitis B, typhoid
fever, rabies, meningococcal meningitis and yellow fever.
Yellow fever vaccine according to the destinations (Table
1). Meningococcal vaccine should be considered for the
associated risk as has been recommended in other previous
World Cups and massive sports events [2,77]. Given the fact
that the 2014 FIFA World Cup Brazil will undoubtedly ensure
that the individual stadiums will be crowded with specta-
tors, and this may increase the risk of the transmission of
disease from asymptomatic infected individuals [77].
Meningococcal outbreaks have occurred during/after other
mass gatherings (e.g. the Hajj). This has led countries such
as Saudi Arabia to require quadrivalent meningococcal
vaccine of all pilgrims. Is important to note that vaccines
available in most parts of the world do not protect against
meningococcus B, a serotype that has caused outbreaks in
Brazil in the past [78].
Regard measles, the interruption of the circulation of
indigenous viruses in Brazil occurred in 2000, and since
then, the country has recorded sporadic reports of illness
related to the imported cases. From the year 2013, measles
cases are occurring in the cities of Fortaleza, Recife, Sao
Paulo, Belo Horizonte, Curitiba, and Brasilia (689 cases),
which will host the FIFA World Cup. Travelers to Brazil
during the World Cup should be vaccinated against measles,
mumps and rubella (MMR) with the aim of preventing the
introduction of the virus in the country, even more
considering the current outbreaks in USA (at California,
New York City and Washington) and Canada (at British
Columbia and Ontario) [79], countries of origin of a signif-
icant number of travelers to Brazil. Measles outbreaks in
the past have demonstrated that unvaccinated persons
place themselves and their communities at risk for measles
and that high vaccination coverage is important to prevent
the spread of measles after importation [80].
Conclusions
As in previous FIFA World Cups, 2014 Brazil will be a major
international sporting and cultural event for the host
country [81]. Brazil is already a popular tourist destination
in Latin America. Healthcare sector administration in Brazil
is prepared to deploy medical resources at any stage of the
event, and for any unexpected health-compromising
events, including but not limited to infectious diseases
and mass casualty events [1,8]. Beyond attention during the
World Cup, travelers to Brazil may encounter Brazil-
endemic infections that could be diagnosed after return-
ing to their countries of origin [32]. Despite pronounced
reductions in the morbidity and mortality due to infectious
diseases over the past six decades, these still pose a public
health problem in Brazil [82]. This review will be helpful to
clinicians and travel medicine practitioners for prevention
and travel-health advice as well for the evaluation of
travel-related conditions in returning travelers from the
Brazil World Cup. Compared to other recent reports [32],
current recommendations would lead to specic regional
destination advice facilitating the assessment of risk ac-
cording to individual and collective itineraries of travelers
going to Brazil for the FIFA World Cup and other related
activities.
8 V. Gallego et al.
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Please cite this article in press as: Gallego V, et al., The 2014 FIFA World Cup: Communicable disease risks and advice for visitors to Brazil
e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004
Mass gatherings and large sporting events such as the
FIFA World Cup and the Olympic Games are associated with
higher population morbidity and increased numbers of
negative health incidents [83]. Visitors to Brazil are
encouraged to take all possible preventive measures to
protect their health prior to departing for any of the 12 host
cities in this South American countries and also to practice
preventive measures during their stay in Brazil.
Conict of interest
The authors have no conict of interest to disclose.
Acknowledgment
The authors thank the reviewers and the Editor-in-Chief,
Dr. Patricia Schlagenhauf for helpful advice, review and
critical comments on the nal version of this manuscript.
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Please cite this article in press as: Gallego V, et al., The 2014 FIFA World Cup: Communicable disease risks and advice for visitors to Brazil
e A review from the Latin American Society for Travel Medicine (SLAMVI), Travel Medicine and Infectious Disease (2014), http://
dx.doi.org/10.1016/j.tmaid.2014.04.004

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