High-risk tourism in areas vulnerable to schistosomiasis mansoni transmission in Brazil

Barreto, Mariana Sena; Gomes, Elainne Christine de Souza; Barbosa, Constança Simões

doi:10.1590/0102-311X00190815

The tourism industry is one of the most important contemporary economic activities and the one with the highest growth rate in the world economy. According to the World Tourism Organization, the number of international trips has grown by 115.4% since 1995, and the forecast is for an additional 58.6% by 2030, when 57% of international arrivals will be at destinations located in emerging economies ¹^,². Brazil belongs to this scenario of expansion in the tourism industry due to the country's multiplicity of natural attractions, having received approximately 6 million international travelers in 2013, adding to the nearly 89 million arrivals of domestic flights ³.

This increase in the tourism industry has contributed to Brazil's economic and social development, with the appreciation of previously economically depressed places. However, in order to enjoy the environments and attract and accommodate visitors, natural landscapes have been modified, harming environmentally fragile areas ⁴. These modifications, imposed on natural spaces and caused by the real estate speculation from tourism's dynamics, expose both the local population and visitors to the risk of acquiring diseases, including schistosomiasis mansoni ⁵^,⁶^,⁷^,⁸^,⁹^,¹⁰.

Schistosomiasis mansoni is one of the most relevant endemic diseases in Brazil, with Schistosoma mansoni as the etiological agent and snails of genus Biomphalaria as intermediate hosts ¹¹. Transmission occurs in 19 of Brazil's states. An estimated 6 million persons are infected, and approximately 25 million individuals are exposed to the risk of acquiring the disease ¹². Due to its magnitude, measures to control schistosomiasis have been conducted in Brazil since 1975 through the Special Schistosomiasis Control Program (PECE), created and implemented by the Inspectorate for Public Health Campaigns (SUCAM), replaced by the Schistosomiasis Control Program (PCE) in the following decade. However, despite efforts, in recent decades the transmission area has expanded to previously unaffected urban and coastal locations, displaying a tendency to changes in the traditional epidemiological pattern of schistosomiasis ¹³^,¹⁴.

Pernambuco State in Northeast Brazil experienced a growing exodus of individuals from rural areas, often parasitized by S. mansoni, to coastal tourist sites, attracted by the abundant supply of jobs in services. They began to live in unhealthy peripheral areas, contaminating the freshwater bodies naturally inhabited by snail vectors of schistosomiasis. During the rainy season breeding sites with infected snails overflow, leading to mass human infection. Scenarios like these have been described in 12 coastal municipalities (counties) in Pernambuco, including the Porto de Galinhas resort in Ipojuca ⁵^,¹⁰^,¹⁵.

Porto de Galinhas achieved high status on world tourist routes in the 1980s. In 2000, 15 schistosomiasis transmission foci were identified, with the first epidemic outbreak of acute cases of the disease in this locality. Introduction of the disease in this resort began with the arrival of rural workers as labor in tourism projects, and the snails were introduced there with the water and sand taken from the Ipojuca River and used as construction materials. The mode of occupation and the modifications in that tourist resort, combined with the adverse climatic and sanitary conditions, were the factors responsible for maintenance of the disease, now considered endemic in Porto de Galinhas ⁵^,¹⁵.

Various coastal tourist sites in Brazil harbor the intermediate hosts of schistosomiasis, and there are reports of transmission of the disease in various coastal destinations in the country ¹⁶^,¹⁷^,¹⁸.

The spread of this disease to coastal localities, although extensive, does not mean that transmission of the disease is any less important in rural endemic areas of Brazil with persistently high schistosomiasis prevalence rates, such areas still maintain the adverse sanitary conditions and sociocultural habits that facilitate the endemic. In recent years, given the growth of tourism in Brazil and the country's environmentally attractive destinations, rural tourism has become a new source of income for many families living in the countryside. The rural tourism industry has encouraged old and economically depreciated agricultural properties to diversify their activities by offering infrastructure for recreation, leisure, and lodging, meanwhile upgrading and revaluing their spaces. However, changes made to the natural environment to help attract tourism, together with the limited investment in sanitation, have produced unhealthy environments that can sustain schistosomiasis transmission, with frequent reports of acute cases in various rural tourist spots, where the flow of visitors and their interaction with structurally imbalanced environments favors spread of the disease across the country and around the world ⁶^,⁷^,⁸^,⁹^,¹⁹.

Travelers exposed to schistosomiasis infection develop the acute form of the disease, since they lack previous contact with the parasite S. mansoni. The acute infection is self-limiting, and travelers can return home without having detected the infection, thus delaying timely treatment and contributing to propagation of the disease in previously unaffected areas ⁹. Tourists can thus become potential disseminators of schistosomiasis, since they move between endemic and non-endemic spaces.

Cases of transmission and spread of schistosomiasis by tourists have been identified in recent years in Europe, where 2014 witnessed the first report of a human case of autochthonous schistosomiasis since elimination of the disease in the 1960s. A 12-year-old German boy was diagnosed with Schistosoma haematobium five months after vacationing with his family in southeastern Corsica, France, where he had bathed in a river ²⁰. Ten more cases were later reported in the same locality ²⁰^,²¹. There are also reports of the migration of patients with schistosomiasis haematobium on the island of Lampedusa, Italy ²². It is further estimated that 2.5% of Spanish tourists may return to Spain infected with Schistosoma, given the significant number of trips to endemic areas ²³. These data show that schistosomiasis is far from being controlled at the local, national, or international level.

All of the above emphasizes the need to investigate the environmental conditions of tourist destinations in Brazil to identify potential health risks, reorganizing and sanitizing the spaces in order to prevent tourists from acquiring schistosomiasis and other vector-borne diseases. Health professionals in tourist locations should be alert to the diagnosis and treatment of local patients, and be aware of the vulnerability to the acute clinical form to which non-immune tourists are exposed. Finally, it is essential to address tourists' health through a set of measures with an inter-sector scope, especially between health surveillance and tourism departments, in a joint effort for the maintenance of healthy tourist environments, valuing Brazil's natural areas and avoiding the exposure of tourists to the risk of acquiring schistosomiasis.

References

¹ World Tourism Organization. Annual report 2014. http://www2.unwto.org/annualreport2014 (acessado em 11/Nov/2015).
» http://www2.unwto.org/annualreport2014
² World Tourism Organization. Tourism highlights 2015. http://mkt.unwto.org/publication/unwto-tourism-highlights-2015-edition (acessado em 11/Nov/2015).
» http://mkt.unwto.org/publication/unwto-tourism-highlights-2015-edition
³ Ministério do Turismo. Anuário estatístico 2015 - ano base 2014. http://www.dadosefatos.turismo.gov.br/dadosefatos/anuario/index.html (acessado em 08/Nov/2015).
» http://www.dadosefatos.turismo.gov.br/dadosefatos/anuario/index.html
⁴ Freitas NR, Souza PAR, Zambra EM, Romeiro MC, Pereira RS. A gestão e a sustentabilidade na atividade turística: uma análise das discussões na última década no Brasil. Revista Brasileira de Ecoturismo 2014; 7:394-411.
⁵ Barbosa CS, Domingues ALC, Abath F, Montenegro SML, Guida U, Carneiro J, et al. Epidemia de esquistossomose aguda na praia de Porto de Galinhas, Pernambuco, Brasil. Cad Saúde Pública 2001; 17:725-8.
⁶ Enk MJ, Amorim A, Schall VT. Acute schistosomiasis outbreak in the metropolitan area of Belo Horizonte, Minas Gerais: alert about the risk of unnoticed transmission increased by growing rural tourism. Mem Inst Oswaldo Cruz 2003; 98:745-50.
⁷ Enk MJ, Caldeira RL, Carvalho OS, Schall VT. Rural tourism as risk factor for the transmission of schistosomiasis in Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 2004; 99 Suppl 1:105-8.
⁸ Massara CL, Amaral GL, Caldeira RL, Drummond SC, Enk MJ, Carvalho OS. Esquistossomose em área de ecoturismo do Estado de Minas Gerais, Brasil. Cad Saúde Pública 2008; 24:1709-12.
⁹ Enk MJ, Amaral GL, Silva MFC, Silveira-Lemos D, Teixeira-Carvalho A, Martins-Filho OA, et al. Rural tourism: a risk factor for schistosomiasis transmission in Brazil. Mem Inst Oswaldo Cruz 2010; 105:537-40.
¹⁰ Barbosa CS, Santos RS, Gomes EC, Araujo K, Albuquerque J, Melo F, et al. Epidemiologia da esquistossomose no litoral de Pernambuco. Rev Patol Trop 2014; 43:436-45.
¹¹ Rey L. Parasitologia. 4a Ed. Rio de Janeiro: Editora Guanabara Koogan; 2008.
¹² World Health Organization. Elimination of schistosomiasis in low transmission areas: Salvador, Bahia. Report of the WHO Informal Consultation. Geneva: World Health Organization; 2009.
¹³ Teixeira MGLC, Paim JS. Os programas especiais e o novo modelo assistencial. Cad Saúde Pública 1990; 6:264-77.
¹⁴ Coura JR, Amaral RS. Epidemiological and control aspects of schistosomiasis in Brazilian endemic areas. Mem Inst Oswaldo Cruz 2004; 99 Suppl 1:13-9.
¹⁵ de Souza Gomes EC, Leal-Neto OB, Albuquerque J, Pereira da Silva H, Barbosa CS. Schistosomiasis transmission and environmental change: a spatio-temporal analysis in Porto de Galinhas, Pernambuco, Brazil. Int J Health Geogr 2012; 11:51.
¹⁶ Guimarães ICS, Tavares-Neto J. Transmissão urbana de esquistossomose em crianças de um bairro de Salvador, Bahia. Rev Soc Bras Med Trop 2006; 39:451-5.
¹⁷ Oliveira DS. Determinação e avaliação dos focos de transmissão esquistossomótica em áreas urbanas do Estado de Sergipe/Brasil [Dissertação de Mestrado]. Aracaju: Universidade Tiradentes; 2011.
¹⁸ Teles HMS, Hiramoto RM, Oliveira JCN, Aveiro JA. Ocorrência de vetores da esquistossomose mansônica no litoral norte do Estado de São Paulo, Brasil. Cad Saúde Pública 2003; 19:1887-91.
¹⁹ de Jesus AR, Silva A, Santana LB, Magalhães A, de Jesus AA, de Almeida RP, et al. Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. J Infect Dis 2002; 185:98-105.
²⁰ Holtfreter MC, Moné H, Müller-Stöver I, Mouahid G, Richter J. Schistosoma haematobium infections acquired in Corsica, France, August 2013. Euro Surveill 2014; 19(22). pii: 20821.
²¹ European Centre for Disease Prevention and Control. Local transmission of Schistosoma haematobium in Corsica, France. Stockholm: European Centre for Disease Preventions and Control; 2014.
²² Bellina L, Maugeri M, Missoni E. Ethical and public health concerns based on the retrospective analysis of referrals for diagnostic parasitology of immigrants and autochthonous population in Lampedusa island (Italy). Trop Med Int Health 2009; 14 Suppl 2:66.
²³ Roca C, Balanzó X, Gascón J, Fernández-Roure JL, Vinuesa T, Valls ME, et al. Comparative, clinico-epidemiologic study of schistosoma infections in travellers and immigrants in Spain. Eur J Clin Microbiol Infect Dis 2002; 21:219-23.

Publication Dates

Publication in this collection
2016

History

Received
18 Nov 2015
Reviewed
22 Jan 2016
Accepted
25 Feb 2016

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] ¹ World Tourism Organization. Annual report 2014. http://www2.unwto.org/annualreport2014 (acessado em 11/Nov/2015).
» http://www2.unwto.org/annualreport2014

[2] ² World Tourism Organization. Tourism highlights 2015. http://mkt.unwto.org/publication/unwto-tourism-highlights-2015-edition (acessado em 11/Nov/2015).
» http://mkt.unwto.org/publication/unwto-tourism-highlights-2015-edition

[3] ³ Ministério do Turismo. Anuário estatístico 2015 - ano base 2014. http://www.dadosefatos.turismo.gov.br/dadosefatos/anuario/index.html (acessado em 08/Nov/2015).
» http://www.dadosefatos.turismo.gov.br/dadosefatos/anuario/index.html

[4] ⁴ Freitas NR, Souza PAR, Zambra EM, Romeiro MC, Pereira RS. A gestão e a sustentabilidade na atividade turística: uma análise das discussões na última década no Brasil. Revista Brasileira de Ecoturismo 2014; 7:394-411.

[5] ⁵ Barbosa CS, Domingues ALC, Abath F, Montenegro SML, Guida U, Carneiro J, et al. Epidemia de esquistossomose aguda na praia de Porto de Galinhas, Pernambuco, Brasil. Cad Saúde Pública 2001; 17:725-8.

[6] ⁶ Enk MJ, Amorim A, Schall VT. Acute schistosomiasis outbreak in the metropolitan area of Belo Horizonte, Minas Gerais: alert about the risk of unnoticed transmission increased by growing rural tourism. Mem Inst Oswaldo Cruz 2003; 98:745-50.

[7] ⁷ Enk MJ, Caldeira RL, Carvalho OS, Schall VT. Rural tourism as risk factor for the transmission of schistosomiasis in Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 2004; 99 Suppl 1:105-8.

[8] ⁸ Massara CL, Amaral GL, Caldeira RL, Drummond SC, Enk MJ, Carvalho OS. Esquistossomose em área de ecoturismo do Estado de Minas Gerais, Brasil. Cad Saúde Pública 2008; 24:1709-12.

[9] ⁹ Enk MJ, Amaral GL, Silva MFC, Silveira-Lemos D, Teixeira-Carvalho A, Martins-Filho OA, et al. Rural tourism: a risk factor for schistosomiasis transmission in Brazil. Mem Inst Oswaldo Cruz 2010; 105:537-40.

[10] ¹⁰ Barbosa CS, Santos RS, Gomes EC, Araujo K, Albuquerque J, Melo F, et al. Epidemiologia da esquistossomose no litoral de Pernambuco. Rev Patol Trop 2014; 43:436-45.

[11] ¹¹ Rey L. Parasitologia. 4a Ed. Rio de Janeiro: Editora Guanabara Koogan; 2008.

[12] ¹² World Health Organization. Elimination of schistosomiasis in low transmission areas: Salvador, Bahia. Report of the WHO Informal Consultation. Geneva: World Health Organization; 2009.

[13] ¹³ Teixeira MGLC, Paim JS. Os programas especiais e o novo modelo assistencial. Cad Saúde Pública 1990; 6:264-77.

[14] ¹⁴ Coura JR, Amaral RS. Epidemiological and control aspects of schistosomiasis in Brazilian endemic areas. Mem Inst Oswaldo Cruz 2004; 99 Suppl 1:13-9.

[15] ¹⁵ de Souza Gomes EC, Leal-Neto OB, Albuquerque J, Pereira da Silva H, Barbosa CS. Schistosomiasis transmission and environmental change: a spatio-temporal analysis in Porto de Galinhas, Pernambuco, Brazil. Int J Health Geogr 2012; 11:51.

[16] ¹⁶ Guimarães ICS, Tavares-Neto J. Transmissão urbana de esquistossomose em crianças de um bairro de Salvador, Bahia. Rev Soc Bras Med Trop 2006; 39:451-5.

[17] ¹⁷ Oliveira DS. Determinação e avaliação dos focos de transmissão esquistossomótica em áreas urbanas do Estado de Sergipe/Brasil [Dissertação de Mestrado]. Aracaju: Universidade Tiradentes; 2011.

[18] ¹⁸ Teles HMS, Hiramoto RM, Oliveira JCN, Aveiro JA. Ocorrência de vetores da esquistossomose mansônica no litoral norte do Estado de São Paulo, Brasil. Cad Saúde Pública 2003; 19:1887-91.

[19] ¹⁹ de Jesus AR, Silva A, Santana LB, Magalhães A, de Jesus AA, de Almeida RP, et al. Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. J Infect Dis 2002; 185:98-105.

[20] ²⁰ Holtfreter MC, Moné H, Müller-Stöver I, Mouahid G, Richter J. Schistosoma haematobium infections acquired in Corsica, France, August 2013. Euro Surveill 2014; 19(22). pii: 20821.

[21] ²¹ European Centre for Disease Prevention and Control. Local transmission of Schistosoma haematobium in Corsica, France. Stockholm: European Centre for Disease Preventions and Control; 2014.

[22] ²² Bellina L, Maugeri M, Missoni E. Ethical and public health concerns based on the retrospective analysis of referrals for diagnostic parasitology of immigrants and autochthonous population in Lampedusa island (Italy). Trop Med Int Health 2009; 14 Suppl 2:66.

[23] ²³ Roca C, Balanzó X, Gascón J, Fernández-Roure JL, Vinuesa T, Valls ME, et al. Comparative, clinico-epidemiologic study of schistosoma infections in travellers and immigrants in Spain. Eur J Clin Microbiol Infect Dis 2002; 21:219-23.