A global systematic review of Chagas disease prevalence among migrants
Graphical abstract
Introduction
One of the current challenges in combating Chagas disease (American trypanosomiasis) is that human migration is changing the distribution of disease in both endemic and non-endemic countries (Gascon et al., 2010, Pinazo and Gascon, 2015). This shift is so great that Chagas disease is now co-classified as both a re-emerging infection and a neglected tropical disease (Hotez et al., 2008, Mackey and Liang, 2012, Mackey et al., 2014; World Health Organization, 2013). Human migration represents both a risk for the re-emergence of new infections in countries with the vector and for the expansion of the geographical distribution of chronic Chagas cases to non-endemic countries.
Caused by the protozoan parasite Trypanosoma cruzi (T. cruzi), Chagas disease results in the largest burden of disease in disability-adjusted-life-years of any parasitic disease in the Americas (Lee et al., 2013; World Health Organization, 2012). Depending on the region, 20–30% of patients chronically infected with Chagas disease go on to develop cardiac and/or gastrointestinal damage and an estimated 10,000 people will die from Chagas each year (World Health Organization, 2010). The morbidity and mortality associated with Chagas disease results in a staggering annual global economic burden of US$7.2 billion (Lee et al., 2013).
The main mode of transmission of T. cruzi to humans is vector borne, which occurs only in the Americas. Traditionally considered a disease of poverty, risk of Chagas disease has been associated with housing in rural areas, of poor construction quality (e.g., palm roof, cracks in the walls), and with domestic pets and livestock in or near the house (Enger et al., 2004, Molina-Garza et al., 2014, Ramsey et al., 2005, World Health Organization, 2002). Coordinated efforts by endemic countries in the 1990's were instrumental in shrinking the domestic vector infestation and thus the population at risk for Chagas disease (Coura and Dias, 2016; Dias and Schofield, 1999, Dias et al., 2002).
Despite the success of spraying campaigns, the disease persists through its alternate transmission mechanisms, primarily congenital and blood transfusion, and to a lesser extent oral ingestion (Alarcon de Noya et al., 2010, Carlier et al., 2015, Coura, 2015; Rassi Jr. et al., 2010). Multiple transmission mechanisms, coupled with the chronic, often asymptomatic nature of the disease and lack of effective and accessible treatment for patients means the burden of disease continues to remain high (Pan American Health Organization, 2014).
Within Latin America, migration into urban areas and an increase in urban poverty has transformed this once rural disease to an urban disease as well (Briceno-Leon and Galvan, 2007). There are an estimated 127 million people living below the poverty line in urban and peri-urban communities in Latin America (Ault, 2007) and sub-standard housing conditions within these urban settings have facilitated the domiciliation of triatomines (Gürtler, 2009, Levy et al., 2006, Medrano-Mercado et al., 2008). A 2013 review of qualitative research on socio-cultural aspects of Chagas disease found that changes in land use may both drive human migration and provide new homes for the vector (Ventura-Garcia et al., 2013). For example, in Peru it was found that human settlement patterns created shantytowns with favorable conditions for triatomines and seasonal agricultural workers may have carried the vector to communities through their work (Bayer et al., 2009). Agricultural workers may be at greater personal risk through exposure to the vector during outdoor labor (Ventura-Garcia et al., 2013, World Health Organization, 2010).
Migration has also changed the distribution of Chagas disease from a health problem only in Latin America, to a global one. As of 2013 there were an estimated 36.7 million people who had migrated out of Latin America and the Caribbean and were residing elsewhere in the world, predominantly in North America (United Nations Department of Economic and Social Affairs, 2013b).
Generally, migrants are at greater risk of infectious diseases because of the existing poverty driving them to migrate and the social and economic inequalities they often face once relocating (Cabieses et al., 2013, Carballo and Nerukar, 2001). A 2013 review of qualitative research uncovered migration as a socio-structural risk factor for Chagas disease (Ventura-Garcia et al., 2013). After migrating, structural barriers to diagnosis and treatment include cost, language, lack of insurance, fear of deportation (in the case of undocumented migrants), and stigma against migrants (Bayer et al., 2009, Jackson et al., 2012, Minneman et al., 2012, Ventura-Garcia et al., 2013).
Current prevalence estimates of Chagas disease in non-endemic countries are largely extrapolations of countrywide prevalence from endemic birth countries multiplied by the proportion of immigrants from that country (Basile et al., 2011, Bern and Montgomery, 2009, Gascon et al., 2010, Schmunis, 2007). While country prevalence estimates provide a good starting point for estimating the burden among migrant populations, there are some substantial drawbacks. First, regional variations in migration rates and Chagas disease burden may be masked by the use of a single prevalence estimate for an endemic country. Secondly, these estimates do not take into account characteristics specific to migrants, who tend to be demographically different from the average person in any given country of origin (Weeks, 2015). Migrants often come from rural areas, have a different age profile (i.e., are younger), and are of a different socioeconomic status than the general population (Bern and Montgomery, 2009).
Determining accurate prevalence estimates of Chagas disease among migrants may enable health systems to more precisely gauge the true burden of disease and target populations most at risk. Further, given the heterogeneity of Chagas disease distribution within countries, there remain questions as to whether migrants are at heightened personal risk for this disease.
Therefore the purpose of this review was to: summarize current seroprevalence estimates of Chagas disease among Latin American migrants, in both endemic and non-endemic settings and compare seroprevalence estimates in migrants to countrywide prevalence estimates. We also report on risk factors for Chagas disease among migrants.
Section snippets
Methods
We conducted a systematic review of the literature from January 2004 to July 2014 using the PubMed and Scopus databases. We also searched relevant grey literature from international and governmental organizations, including the Pan American Health Organization (PAHO), World Health Organization (WHO), and the U.S. Centers for Disease Control and Prevention. Search terms included combinations of the following keywords: (1) Chagas; American trypanosomiasis; or T. cruzi; (2) migra*; mobil*;
Description of included and excluded studies
After duplicates were removed, the initial search identified a total of 311 original articles and an additional 9 references were identified through other sources. Of these records, 246 did not meet initial inclusion criteria (Fig. 1). A total of 74 articles were included for full text review and 23 met the inclusion criteria for the final analysis. Among the excluded articles: 5 did not contain original prevalence estimates; 18 had selection bias (i.e., tropical disease hospital sample or
Discussion
An estimated 94–96% of migrants living with Chagas disease in non-endemic areas are unaware of their disease (Basile et al., 2011). Underestimating the burden of disease among Latin American migrants likely means a continued lack of priority for a neglected disease and migrant health generally.
We found a trend that the prevalence of Chagas disease in migrant groups, when stratified by birth country, was generally higher than endemic countrywide estimates of prevalence. In non-endemic countries,
Conclusions
Our findings from this literature review, along with recent work by others to establish more accurate prevalence estimates in Europe, are that Chagas disease estimates among migrants are generally poor (Requena-Mendez et al., 2015). No longer only a disease of Latin America, control of Chagas disease now requires the joint collaboration of endemic and non-endemic countries.
Despite challenges, the benefit of better estimates and surveillance are manifold and include improved distribution of
Acknowledgements
Erin Conners was supported by a UC MEXUS dissertation research grant titled “The Potential Role of Migration in Chagas Disease Expansion” and the University of California, San Diego, Center for AIDS Research (CFAR), an NIH-funded program (P30 AI036214), which is supported by the following NIH Institutes and Centers: NIAID, NCI, NIMH, NIDA, NICHD, NHLBI, NIA, NIGMS, and NIDDK.
References (77)
- et al.
Large urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela
J. Infect. Dis.
(2010) Pan American Health Organization's Regional Strategic Framework for addressing neglected diseases in neglected populations in Latin America and the Caribbean
Mem. Inst. Oswaldo Cruz
(2007)- et al.
Prevalence of Trypanosoma cruzi infection and vertical transmission in Latin-American pregnant women in a health area of Biscay
Enferm. Infecc. Microbiol. Clin.
(2013) - et al.
Prevalence of Trypanosoma cruzi infection in pregnant Latin American women and congenital transmission rate in a non-endemic area: the experience of the Valencian Health Programme (Spain)
Epidemiol. Infect.
(2012) - et al.
Chagas disease in European countries: the challenge of a surveillance system
Euro. Surveill.
(2011) - et al.
Chagas disease, migration and community settlement patterns in Arequipa, Peru
PLoS Negl. Trop. Dis.
(2009) - et al.
An estimate of the burden of chagas disease in the United States
Clin. Infect. Dis.
(2009) - et al.
The social determinants of Chagas disease and the transformations of Latin America
Mem. Inst. Oswaldo Cruz
(2007) - et al.
Interval estimation for a binomial proportion – comment – rejoinder
Stat. Sci.
(2001) - et al.
Congenital Chagas disease: diagnostic and clinical aspects in an area without vectorial transmission, Bermejo, Bolivia
Acta Trop.
(2008)
Changing patterns of migration in Latin America: how can research develop intelligence for public health?
Rev. Panam. Salud Publica
Migration, refugees, and health risks
Emerg. Infect. Dis.
Congenital Chagas disease: an update
Mem. Inst. Oswaldo Cruz
The main sceneries of Chagas disease transmission. The vectors: blood and oral transmissions—a comprehensive review
Mem. Inst. Oswaldo Cruz
Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery
Mem. Inst. Oswaldo Cruz
Epidemiologic and laboratory findings from 3 years of testing United States blood donors for Trypanosoma cruzi
Transfusion
Chagas' disease, foetal maternal transmision and experience in our hospital
Enferm. Emerg.
The evolution of Chagas disease (American trypanosomiasis) control after 90 years since Carlos Chagas discovery
Mem. Inst. Oswaldo Cruz
The impact of Chagas disease control in Latin America: a review
Mem. Inst. Oswaldo Cruz
Perinatal Screening for Chagas Disease in Southern Texas
Testing blood donors for Chagas disease in the Paris area, France: first results after 18 months of screening
Transfusion
Evaluation of risk factors for rural infestation by Triatoma pallidipennis (Hemiptera: Triatominae), a Mexican vector of Chagas disease
J. Med. Entomol.
Update on seroprevalence of anti-Trypanosoma cruzi antibodies among blood donors in northeast Mexico
Am. J. Trop. Med. Hyg.
Chagas disease in Spain, the United States and other non-endemic countries
Acta Trop.
Hispanic ethnicity, race and blood donation in the United States
Transfus. Med.
Prevalence of Trypanosoma cruzi antibodies in immigrants living in Valencia (Spain)
Enfermedades Emerg.
Sustainability of vector control strategies in the Gran Chaco region: current challenges and possible approaches
Mem. Inst. Oswaldo Cruz
The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination
PLoS Negl. Trop. Dis.
Economic evaluation of Chagas disease screening in Spain
Acta Trop.
Metabolic, mental health, behavioural and socioeconomic characteristics of migrants with Chagas disease in a non-endemic country
Trop. Med. Int. Health
Prevalence, clinical staging and risk for blood-borne transmission of chagas disease among latin American migrants in Geneva, Switzerland
PLoS Negl. Trop. Dis.
Congenital transmission of chagas disease in Latin American immigrants in Switzerland
Emerg. Infect. Dis.
Global economic burden of Chagas disease: a computational simulation model
Lancet Infect. Dis.
Chagas disease, France
Emerg. Infect. Dis.
Experience of targeted screening of Chagas disease in Île-de-France
Bull. Soc. Pathol. Exot.
Periurban Trypanosoma cruzi-infected Triatoma infestans Arequipa, Peru
Emerg. Infect. Dis.
Prevalence of American tripanosomiasis in pregnant women from a health area of Valencia, Spain 2005–2007
Rev. Esp. Salud Publica
On the possibility of autochthonous chagas disease in Roraima, Amazon Region, Brazil, 2000–2001
Rev. Inst. Med. Trop. Sao Paulo
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