The 2014 FIFA World Cup: communicable disease risks and advice for visitors to Brazil--a review from the Latin American Society for Travel Medicine (SLAMVI).

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Travel Medicine and Infectious Disease (2014) xx, 1e11

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevierhealth.com/journals/tmid

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 Scientific 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 specific 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 influenza, measles but also tropical endemic diseases. In anticipation of increased travel, a panel of experts from the Latin American Society for Travel Medicine (SLAMVI) developed the current recommendations regarding the epidemiology 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 significant 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.: þ57 300 884 74 48. E-mail addresses: [email protected], [email protected] (A.J. Rodriguez-Morales). http://dx.doi.org/10.1016/j.tmaid.2014.04.004 1477-8939/ª 2014 Elsevier Ltd. All rights reserved.

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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V. Gallego et al. 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 infections. Other important recommendations for travelers should focus on preventing water and food-borne diseases such as hepatitis A, typhoid fever, giardiasis and traveler’s diarrhea. Sexually transmitted diseases (STD) should be also mentioned and the use of condoms advocated. 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 infectious diseases in travelers returning to their countries of origin. ª 2014 Elsevier Ltd. All rights reserved.

Introduction The FIFA World Cup is to be held in Brazil for the second time in 2014 (the first 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 international gatherings, this event poses specific challenges, 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 influenza [2], but also tropical diseases that are endemic in Brazil, such as malaria, dengue, leishmaniasis, among others. In addition, such high-profile 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 PanAmerican 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 intelligence 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 specific challenges not only to implementing control measures due to the mobility of the attendees 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 conditions, particularly at the host cities, the Federal Government 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 (Caˆmara Tema´tica de Sau´de), with the objective to promote interaction between different government sectors, define 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 implementation of new health strategies, for example the inclusion of bags with health aid devices and defibrillators 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 recommendations constitutes a scientific 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).


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The 2014 FIFA World Cup

About Brazil Brazil is the largest country in both South America and the Latin American region. It is the World’s fifth largest country, 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 km2 (3,287,612 sq mi), including 55,455 km2 (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 official 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 topography 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 five geopolitical regions (north, northeast, central west, southeast and south) (Fig. 1), one Federal district (which contains the capital city, Brası´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].

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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 municipalities 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 Santare ´m. There is no transmission in Bele ń, 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 Espı´rito Santo state, in summer (December until March). No transmission 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 regard the potential need for chemoprophylaxis. If indicated, atovaquoneeproguanil, doxycycline or mefloquine are recommended. As in most of Latin America, Plasmodium falciparum is resistant to chloroquine. In Brazil the first 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.


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V. Gallego et al.

Table 1 Specific 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

Host City Belo Horizonte Brasilia Cuiaba ´ Curitiba Fortaleza Manaus Natal Porto Alegre Recife Rio de Janeiro Salvador Sao Paulo Statesa North Region Acre Amapa ´ Amazonas Para ´ Rondo ˆnia Roraima Tocantins Northeast Region Alagoas Bahia Ceara ´ Maranha õ Paraı´ba Pernambuco Piauı´ Rio Grande do Norte Sergipe Central West Region Federal District Goia ´s Mato Grosso Mato Grosso do Sul Southeast Region Espı´ritu Santo Minas Gerais Rio de Janeiro Sa õ Paulo South Region Parana ´ Rio Grande do Sul Santa Catarina a b

Endemic infectious diseases of concern for travelers to Brazil

Recommendations of

Malariab

Dengue

Leishmaniasis

Schistosomiasis

Yellow fever vaccine

Vector avoidance measures

No No No No No Yes No No No No No No

Yes Yes Yes No Yes Yes Yes No Yes Yes Yes Yes

No No No No No No No No No No No No

No No No No No No No No No No No No

Yes Yes Yes No No Yes No No No No No No

Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

Yes Yes Yes Yes Yes Yes Yes



No No No No No No No



No No

Yes Yes

Yes Yes

Yes Yes

Yes Yes

No Yes, west No No No No No



No No Yes Yes No Yes Yes

No Yes, south and west No Yes No No Yes, south No No


No No Yes, some municipalities No

Yes Yes Yes

No No Yes

Yes No No

Yes Yes Yes

Yes Yes Yes

Yes

No

No

Yes

Yes

No No No No

Yes Yes Yes Yes

No Yes No No

No Yes No No

Yes, north Yes No Yes, northwest

Yes Yes Yes Yes

No No No

No No No

No No No

No No No

Yes, west Yes, west Yes, west

Yes Yes Yes

Excluding capital cities. Risk areas, but currently low transmission during JuneeJuly.


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Fig. 2 Evolution of the number of malaria cases reported in Brazil, 2005e2012. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

of treatment for P. falciparum malaria is artemetherlumefantrine or artesunate plus mefloquine. 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 influenza-like symptoms, including chills, headache, 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 syndrome, 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 confirmed 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 malaria and about need to seek care and inform the clinician about possible malaria exposure in case symptoms indicative 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 malaria 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 Maranha õ (northeastern region), Minas Gerais (southeastern region) and the southern

5 municipalities of Piauı´ state (northeastern region), the western and southern area of the state of Bahia (northeast region), north of Espirito Santo (southeastern region), northeastern area of Sa õ 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 confirmed cases with 9 deaths (43% case fatality 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 Rıó 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 indications 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). Accommodation 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 disease 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 105, 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 Catarina 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


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V. Gallego et al. Table 2 Dengue incidence rates (cases/100,000pop) in Brazil by regions and states, 2011e2013. Region and state

2011

2012

2013

North Region Rondo ˆnia Acre Amazonas Roraima Para ´ Amapa ´ Tocantins Northeast Region Maranha õ Piauı´ Ceara ´ Rio Grande do Norte Paraı´ba Pernambuco Alagoas Sergipe Bahia Southeast Region Minas Gerais Espı´rito Santo Rio de Janeiro Sa õ Paulo South Region Parana ´ Santa Catarina Rio Grande do Sul Central West Region Mato Grosso do Sul Mato Grosso Goia ´s Federal District Brasil

752.6 206 2571.70 1779.20 322.1 253.8 418.7 855.4 368 179.1 322.6 747.8 731.4 334.6 251.2 285.5 189.9 282.6 449.6 205.9 1147.60 1036.80 278.4 131.4 339.3 2.8 3.4 369.5 347.5 202.5 565.6 129.4 400.5

257.9 207 315.4 143.9 399.1 207.7 224.6 819.4 413.5 79.3 387.7 637.1 891.5 229.9 356.1 888.4 215.9 342 308.6 148.4 334.3 1116.20 69.6 17.2 42.6 1.5 1.6 471.5 367.3 1054.70 398.3 54.2 303.9

301.3 544.4 364.9 467 195.3 117.3 235.4 616.4 273.3 53.4 156.5 355.7 529.6 342.3 93.6 295.6 37.9 413.1 1097 2044.6 1796.9 1303.8 511 241.2 624 5.8 4 1806.1 3062.3 1128.7 2233.6 428 731.5

cruzi-infected feces come in contact with food and beverages (eg. Ac ¸ai, local fruit, juice; sugar cane juice) that are undercooked, unpasteurized and/or raw. Seven to 8 outbreaks (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 Barcarena, Abaetetuba (Para ´ state), Pau Da ´rco, Mojuı´ dos Campos, close to Santare ´m (also in Para ´ state) (Fig. 1). Reports of consumption of contaminated ac ¸aı´ 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 recommended to avoid undercooked, unpasteurized and/or raw foods and beverages.

Dermatological conditions (Leishmaniasis, Cutaneous larva migrans, Rickettsiosis) Arthropods are a significant 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 exposure. 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 sandflies 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 reported 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 flies by using personal protective measures. Travelers should be advised to: avoid outdoor activities, especially from dusk to dawn, when sand flies 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 manufacturer’s instructions; 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 flies, which are weak fliers [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 acquired 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 serpiginous, erythematous track appears in the skin and is associated 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


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Fig. 3 A typical case of cutaneous larva migrans showing the serpiginous and erythematous track in the skin.

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 cutaneous manifestations. These are usually transmitted from the host-animal reservoirs human through the bite of a wide variety arthropods such as lice, fleas 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. Transmission 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, Espı´ritu Santo, Rio de Janeiro, Parana ´ and Santa Catarina) [44]. The risk for travelers is considered 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 significant risk include Bahıá and Minas Gerais (Fig. 1) as well Sergipe, Alagoas, Pernambuco, Paraiba and the state of Rıó 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

7 HIV/AIDS cases in Latin America (with over half-million people 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 STD and transmitting it, both in their home country and in the visiting country [51e53]. Condom use should be recommended for travelers with the potential to engage in sexual relationships when visiting Brazil. On December 5, 2013, UNAIDS launched the campaign: “Protect the goal”. 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, influenza, hantavirus and leptospirosis Tuberculosis incidence in Brazil is estimated in around 25 cases/100,000pop. In 2011, 70,000 new cases were reported. In 2010, 4600 deaths due to tuberculosis were reported. Tuberculosis is the fourth cause of death in the country and the first 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]. Influenza is the most common vaccine preventable disease in travelers but only few travelers have influenza vaccine. In southern Brazil, AprileAugust is the influenza 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 influenza-like illness; of these, 37,120 had samples collected and 6421 tested positive: 1690 (26%) influenza A, 567 (9%) influenza B, 277 (4%) parainfluenza 1571 (9%) parainfluenza 2589 (9%) parainfluenza 3742 (12%) adenovirus, and 1985 (31%) respiratory syncytial virus [60]. Hantavirus is also a significant 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 reservoirs of hantavirus in the Atlantic Forest and Cerrado biomes of Brazil. N. lasiurus showed a wide potential distribution 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.


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8 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. Traveler’s diarrhea and foodborne 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 officers during the inspection of facilities where food services. This has been considered an innovative preventative sanitary action because it was created based on scientific information, statistical calculation and on risks of foodborne diseases 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, influenza, 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 influenza and hepatitis B vaccines (14%, 11%) [59]. Recommended vaccines include hepatitis A (if not included as routine vaccine

V. Gallego et al. 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 spectators, 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 significant 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 Brazilendemic infections that could be diagnosed after returning 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 specific regional destination advice facilitating the assessment of risk according to individual and collective itineraries of travelers going to Brazil for the FIFA World Cup and other related activities.


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The 2014 FIFA World Cup 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.

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Conflict of interest The authors have no conflict of interest to disclose.

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Acknowledgment

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The authors thank the reviewers and the Editor-in-Chief, Dr. Patricia Schlagenhauf for helpful advice, review and critical comments on the final version of this manuscript.

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